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Plate 1. Adult captive gharials at the Madras Crocodile Bank. Note the ghara, the nasal excrescence, of the male gharial. Plate 2. The right gonad, macroscopically undifferentiated, of a juvenile Nile crocodile can be seen between the spleen and the right kidney. The left gonad is hidden by the mesentery. The yellowish adrenals are almost completely obscured by the paler gonads. Plate 3. The dark-brown right thyroid situated laterally of the right bronchus. The pale right parathyroid is visible slightly caudally of the thyroid on the right aortic arch, medially of the precaval vein. Plate 4. Fighting male Nile crocodiles on a crocodile farm in South Africa. Plate 5. Oral cavity, gular valve and pharynx exposed after the ventral skin has been removed and the tongue has been cut loose from the mandibles. Plate 6. Cutting lines for a belly skin.

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Plate 7. Spectacled caiman hatchling with the greyish-white crusty lesions of caiman pox on the dorsal and lateral surfaces of head, body, tail and limbs. Plate 8. Nile crocodile hatchling with ventral, dark-brown crocodile pox lesions in patterns suggesting bite marks. Plate 9. Reddening of the ventral skin of the hind legs and around the cloaca of a juvenile Nile crocodile with septicaemia. Plate 10. Right elbow joint of a juvenile Nile crocodile with exudative arthritis. Plate 11. Heart of an adult Nile crocodile with exudative epicarditis. Plate 12. Hepatozoon sp. gametocyte in a red blood cell of a Nile crocodile.

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Plate Plate Plate Plate Plate Plate

13. Ascaridoids in the stomach of an adult wild-caught Nile crocodile. 14. Juvenile Nile crocodile with fat necrosis involving the thoracic and abdominal fat deposits. 15. Fat necrosis: hardened yellow fat between the tail muscles of a Nile crocodile. 16. Renal gout in a juvenile Nile crocodile with deposits of uric acid in the pelvic portions of the renal folds. 17. Close-up of winter sores on the ventral surface of the tail of a juvenile Nile crocodile. 18. Advanced case of stress dermatitis with lesions affecting all parts of the body.

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Plate Plate Plate Plate Plate Plate

19. Large fungal granuloma on the right hind foot of an adult captive Indo-Pacific crocodile. 20. Exudative enteritis causing the intestine to be grossly distended by the fibrinous exudate. 21. Haemorrhagic enteritis in a juvenile Nile crocodile. 22. Tonsillitis in a juvenile Nile crocodile. 23. Laryngitis in a juvenile Nile crocodile. 24. Lacrimal cyst under the eye of a captive Nile crocodile (photo Marc Gansuana).

Crocodiles

Biology, Husbandry and Diseases

Crocodiles
Biology, Husbandry and Diseases

F.W. Huchzermeyer
Onderstepoort Veterinary Institute, South Africa

CABI Publishing

CABI Publishing is a division of CAB International CABI Publishing CAB International Wallingford Oxon OX10 8DE UK Tel: +44 (0)1491 832111 Fax: +44 (0)1491 833508 E-mail: cabi@cabi.org Website: www.cabi-publishing.org CABI Publishing 44 Brattle Street 4th Floor Cambridge, MA 02138 USA Tel: +1 617 395 4056 Fax: +1 617 354 6875 E-mail: cabi-nao@cabi.org

CAB International 2003. All rights reserved. No part of this publication may be reproduced in any form or by any means, electronically, mechanically, by photocopying, recording or otherwise, without the prior permission of the copyright owners. A catalogue record for this book is available from the British Library, London, UK. Library of Congress Cataloging-in-Publication Data Huchzermeyer, F. W. (Fritz W.) Crocodiles : biology, husbandry and diseases / by F. W. Huchzermeyer. p. cm. Includes bibliographical references (p. ). ISBN 0-85199-656-6 1. Crocodile farming. 2. Crocodiles. 3. Captive reptiles. I. Title. SF515.5.C75 H83 2003 639.3 982--dc21 2002013734 ISBN 0 85199 656 6 Typeset in Palatino by Columns Design Ltd, Reading. Printed and bound in the UK by Biddles Ltd, Guildford and Kings Lynn.

Contents

Foreword Disclaimer Introduction 1 Crocodiles and Alligators The Species of Crocodilians Crocodilian Anatomy Crocodilian Physiology Crocodilian Biochemistry Crocodilian Behaviour Examination of Crocodiles and Clinical Procedures Clinical Examination Post-mortem Examination Medication Surgical Interventions Important Aspects of Crocodile Farming Nutrition Incubation of Crocodile Eggs Rearing Breeding Slaughter Crocodiles in Zoos and Private Collections Animal Welfare Diseases of Eggs and Hatchlings Diseases of the Egg Diseases of the Yolk-sac Hatchling Diseases Congenital Malformations Transmissible Diseases Viral Infections Bacterial Infections Fungal Infections Parasitic Protozoa Metazoan Endoparasites Ectoparasites

vii viii ix 1 1 6 32 47 52 57 57 75 86 91 98 98 102 107 118 123 133 136 139 139 142 145 148 157 157 163 176 182 192 203
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Contents

Non-transmissible Diseases Nutritional Diseases Poisoning Multifactorial Diseases Organ Diseases and Miscellaneous Conditions Skin Diseases Eye Diseases Diseases of the Digestive System Diseases of the Urogenital System Diseases of the Nervous System Diseases of the Circulatory System Diseases of the Respiratory System Diseases of the SkeletalMuscular System Diseases of the Endocrine System Miscellaneous Pathological Conditions

211 211 221 226 240 240 245 247 263 266 268 270 272 274 277 292 323

References Index

Foreword

Crocodilians have been the subject of international study for hundreds of years. Research on their biology began appearing in the literature during the 1800s, increased considerably in the 1920s and then really took off after the mid-1950s, when funding for academic research became more readily available. These early studies concentrated on various aspects of population dynamics of the species in the wild, and of crocodilians kept in display centres and zoos. Husbandry and diseases of crocodiles received early attention by zoo veterinarians and keepers, but interest in these matters took a dramatic turn upwards once ranching and farming of the species became a serious business, worth hundreds of millions of dollars. I well remember some 25 years ago how at meetings of the Crocodile Specialist Group (CSG), someone would mention seeing blemishes on crocodile skins and how this would drastically decrease the value of the skins. Soon dozens of husbandry problems and diseases came to the fore and it became imperative that the issues be looked at in a systematic and deliberate fashion. More and more researchers became interested in the eld, and by the year 2000 the CSG had decided to establish, with the encouragement and leadership by Dr Fritz Huchzermeyer, a veterinary group within the CSG. I am delighted to see that Dr Huchzermeyer has put pen to paper and produced this most important and valuable book on husbandry and diseases of crocodilians. It will have many avid readers. Professor Harry Messel Chairman, CSG

vii

Disclaimer

Although every effort has been made in the collection and presentation of facts the author cannot accept any responsibility for damages arising from actions based on information contained in this book.

viii

Introduction

This book has been written for veterinarians, scientists, wildlife ofcials, students and crocodile farmers. The knowledge was gained mainly by my work over many years with farmed Nile crocodiles, some work with wild and wild-caught African dwarf crocodiles in the Congo Republic and, in addition, by the study of the available literature, which embraces most of the other crocodilian species as well. I believe this to be the rst comprehensive book on crocodile diseases. Being a pathologist, poultry pathologist, and not a clinician, I placed the emphasis in this book on the diagnosis and treatment, or rather prevention, of diseases as they occur on crocodile farms. However, an effort has been made to cover all clinical aspects as well. I believe that my avian background has helped me to grasp the peculiarities of crocodilian physiology and pathology, while my poultry background has guided me towards a herd health approach. Diseases cannot be understood without a background knowledge of normal body functions, nor without knowledge of farming conditions. These are therefore treated in a somewhat introductory fashion in the rst and third part, without any claim of completeness. Wherever possible, common names have been used as well as scientic names, in an effort to make the book more accessible. Unless emphasized specically the term crocodiles is used to denote all crocodilians (see Chapter 1). Basically we know very little about crocodiles and their diseases. Research into their biology is carried out and funded in the course of normal biological studies and conservation efforts. However, most veterinary research is centred on domestic animals and may at best involve some of the major wildlife species, possibly stimulated by a need to protect the inhabitants of national parks and zoological gardens. The crocodile farming and ranching industries in the various countries are in competition with each other and are most unlikely to be able to provide funding for a concerted and specialized veterinary research effort. There are no catastrophic crocodile diseases, and consequently veterinary research will always be regarded as not so important. I had the good fortune that the Poultry Section of the Onderstepoort Veterinary Institute (OVI) was closed a few years before my retirement and that I was allowed then to devote all my time to crocodile work. For some years I had some nearby crocodile farms submit practically all their mortalities. The many post-mortems carried out during that time and the generous permission to make full use of the Institutes library, even up to the present, have laid a foundation of knowledge, on which I became condent to tackle writing this book. The past and present directors of the OVI, Dr D.W. Verwoerd, Dr G.R. Thomson, Dr S.T. Cornelius and Dr F.T. Potgieter, are thanked for the provision of an ofce for my use and continued access to the Institutes infrastructure since my retirement, as well as for their continued interest in my work. The secretary of the now also defunct Pathology Section of the OVI, Mrs Mara Stoltz, has always been at hand to solve computer and program problems
ix

Introduction

most speedily and efciently, and Mr D. Swanepoel of the Institutes library and his staff have been most helpful in trying to procure even the most obscure items of literature. Over the years I have been most fortunate in having been able to draw on the knowledge of many colleagues, for which I want to express my gratitude. Many crocodile farmers in southern Africa have welcomed me on their farms and have allowed me to study their animals in their environment. Dr Jenny Turton and Dr Jane Walker reviewed parts of the manuscript and helped me to overcome some of my language problems. To all go my heartfelt thanks. And, last but not least, I have to thank my wife Hildegard, who not only put up with my periods of withdrawal while writing, but always showed a keen interest in my work and encouraged me to carry on. F.W. Huchzermeyer Pretoria June 2002

Chapter 1
Crocodiles and Alligators

The Species of Crocodilians


The crocodilians are classied as reptiles, together with lizards, snakes, tuataras and chelonians (tortoises, terrapins and turtles note that the Americans use the term turtles for all chelonians), because of their exothermia and their skin architecture. However, many features, particularly behaviour (vocalizations and parental care), heart morphology and fat body, clearly separate them from the other reptiles. All living crocodilians are grouped in the family Crocodylidae. They occur in a broad band around the globe in the tropics and subtropics of the Old and New World. At present the distinctions between subfamilies, genera and species are based mainly on anatomical features, particularly of the skull, and on scale patterns of the skin. DNA analyses may, in the near future, add new information and cause some revisions (Densmore and Owen, 1989; Ray et al., 2001; White and Densmore, 2001). The following details were taken mainly from Ross and Magnusson (1989). Please note that several common names can be in use for any one species. An effort has been made in this book to use only one common name per species, as listed below. Many synonyms of the scientic names can be found in the older literature. Where this

literature is cited, these synonyms have been replaced in most cases by the current names.

Crocodiles The subfamily Crocodylinae contains three genera: Crocodylus (the true crocodiles, with 13 species), Osteolaemus and Tomistoma (each with one species). The genus Crocodylus:
C. rhombifer C. moreletii C. acutus C. cataphractus Cuban crocodile Morelets crocodile American crocodile African slendersnouted crocodile (Fig. 1.1) Nile crocodile (see Fig. 1.7) Orinoco crocodile Indo-Pacic crocodile Johnstons crocodile Mugger (Fig. 1.2) Cuba Central America Central America Africa

C. niloticus C. intermedius C. porosus C. johnsoni C. palustris

C. siamensis Siamese crocodile C. mindorensis Philippine crocodile C. novaeguineae New Guinea crocodile C. raninus Bornean crocodile

Africa and Madagascar South America Asia and Australia Australia Indian subcontinent Asia Philippines New Guinea Borneo (see Ross, 1990; Ross et al., 1998) 1

CAB International 2003. Crocodiles: Biology, Husbandry and Diseases (F.W. Huchzermeyer)

Chapter 1

Due to a consistent spelling error in its original description, the scientic name of Johnstons crocodile is C. johnsoni. As the rules of nomenclature do not allow a subsequent correction, the original spelling of the scientic name must be retained. The wide distribution of C. porosus in the

Indo-Pacic area, C. niloticus throughout Africa and Madagascar, and C. acutus in Central America is probably due to their ability to tolerate varying degrees of salinity. This has allowed them to spread to different river systems and even islands, unlike more localized species that do not have any salt

Fig. 1.1. Captive Crocodylus cataphractus at the St Lucia Crocodile Centre.

Fig. 1.2. Captive Crocodylus palustris at the Madras Crocodile Bank.

Crocodiles and Alligators

tolerance. It therefore appears to be incorrect to use the names saltwater and freshwater crocodiles for C. porosus and C. johnsoni, respectively, outside Australia. The genus Osteolaemus:
O. tetraspis Dwarf crocodile Africa

The genus Tomistoma:


T. schlegelii False gharial (Fig. 1.5) Asia

Alligators The subfamily Alligatorinae contains four genera: Alligator (the true alligators, with two species), Caiman (the caimans, with two species), Palaeosuchus (the dwarf caimans,

This has two subspecies, as follows:


O. t. tetraspis from coastal West Africa (Fig. 1.3); and O. t. osborni from the Congo basin (Fig. 1.4).

Fig. 1.3. Captive juvenile Osteolaemus tetraspis tetraspis at the St Lucia Crocodile Centre. Their colouring is yellow and black, while that of O. t. osborni hatchlings is green and black.

Fig. 1.4. Young adult wild-caught Osteolaemus tetraspis osborni trussed up for transport to the market.

Chapter 1

Fig. 1.5. Captive Tomistoma schlegelii on a farm in Kuching, East Malaysia.

with two species) and Melanosuchus (the black caiman, with only one species). The genus Alligator:
A. mississippiensis A. sinensis American alligator USA Chinese alligator China

The genus Caiman:


C. latirostris C. crocodilus Broad-snouted caiman Common caiman (Fig. 1.6) South America South America

Fig. 1.6. Juvenile Caiman crocodilus on a farm in So Paulo State, Brazil.

Crocodiles and Alligators

The genus Palaeosuchus:


P. palpebrosus P. trigonatus Cuviers dwarf caiman Schneiders dwarf caiman South America South America

The genus Melanosuchus:


M. niger Black caiman South America

Gharials The subfamily Gavialinae only has one genus, Gavialis, with a single species. The genus Gavialis:
G. gangeticus Gharial (Plate 1) Indian subcontinent

live further north than caimans and crocodiles in both North America and in China. 2. In alligators and caimans the teeth of the lower jaw t into pits in the upper jaw, consequently when the mouth is closed no mandibular teeth are visible. In crocodiles the fourth mandibular tooth ts into a notch in the upper jaw and thus remains visible when the mouth is closed (Fig. 1.7). 3. Crocodiles and gharials have sensory pits in the ventral scales (Fig. 1.8). These are absent in alligators and caimans. This is one of the important features used in the species identication of goods made from crocodilian leather.

Wild or captive? This refers to the description of the different ways in which the crocodiles are living or kept. Wild Crocodiles in the wild may be either left entirely to their own devices or subjected to a certain degree of management. They are hardly ever seen to be suffering from disease

Differences between crocodiles and alligators This question is asked quite regularly. There are many anatomical and physiological differences, but for the purposes of this book it will sufce to name only three reasonably obvious ones: 1. Alligators are more cold resistant than caimans and crocodiles. They can therefore

Fig. 1.7. Adult Nile crocodile on a farm in South Africa. Note the visible fourth mandibular tooth in its maxillar notch.

Chapter 1

Fig. 1.8. Sensory pits in the ventral skin of Crocodylus palustris.

or dying, and often they live in such remote areas that suitable specimens rarely reach the laboratory (see also p. 239). Captive Crocodiles kept in zoos and other collections without a productive goal are referred to as captive. They may be bred or exhibited only, but they may also be subjected to scientic studies. Wild-caught Crocodiles caught in the wild and kept for a short period restrained for the purpose of sample collection or transported alive to a market, where they are slaughtered. They are under very severe stress which may affect many of their physiological and biochemical parameters. Such animals should be referred to as wild-caught. Ranched Crocodiles kept on farms for commercial (productive) purposes, but either hatched from eggs collected in the wild or having been collected as hatchlings, are referred to as ranched. Their diseases are substantially

the same as those of farmed crocodiles, except for their closer contact with wild populations, which may constitute a natural reservoir of crocodile-specic infectious agents. Farmed Crocodiles hatched from eggs laid by breeding stock kept on a farm for commercial purposes are called farmed crocodiles. The on-farm breeding of these crocodiles allows the genetic selection for certain productive parameters. These animals no longer have a direct link to the wild. Their only contribution to the conservation of wild crocodiles may be to keep commodity prices low, thereby lowering the incentive for poaching. However, they may also provide a substantial additional gene pool. Where such crocodiles are farmed far away from wild crocodile populations the incidence of crocodile-specic infectious diseases is usually very low.

Crocodilian Anatomy
The aim of this section is to provide sufcient information for the normal functions of

Crocodiles and Alligators

the body to be understood and for the recognition of the organs during post-mortem examinations. This information is based largely on my own experience with Nile crocodiles. For a reasonably detailed and accurate study of the anatomy of the American alligator see Chiasson (1962). We are still waiting for a standard textbook on crocodilian anatomy. A dissection guide for post-mortem examinations is given in Chapter 2 (p. 75).

roughly between the orbits and the supertemporal fossae. The articulation of the jaw is caudal to the atlanto-occipital joint, allowing the jaws to open extremely widely (Fig. 1.11). Vertebrae The cervical and thoracic vertebrae have ribs. The cervical ribs lie alongside the vertebral column pointing caudally, but only the thoracic ribs connect with the sternum. A cartilaginous portion in the midrib allows exibility for collapsing the thorax during deep diving. The lumbar vertebrae do not have ribs, but the sacral ones do. Dorsally all the vertebrae bear neural spines; and ventrally, chevron bones, which point in an obliquely caudal direction, are attached to the caudal vertebrae. A brous membrane bearing abdominal ribs (gastralia) connects the sternum with the os pubis and supports the abdominal viscera. Legs The pectoral girdle, consisting of the scapula, coracoid and sternum, together with the rst

The skeleton Skull The pitted appearance of the dorsal skull surface (Fig. 1.9) is due to its fusion with the skin. There are three pairs of foramina dorsally on the skull: the external nares opening into one nasal orice, the orbits and the supertemporal fossae (Fig. 1.9). On the ventral aspect, almost at the same level, are the anterior palatine foramina (foramen), the posterior palatine foramina and, partially hidden, the internal nares (Fig. 1.10). The cranium, which houses the brain, lies

Fig. 1.9. Pitted appearance of the skull bones of a mature Nile crocodile, dorsal aspect.

Chapter 1

Fig. 1.10. Ventral aspect of the skull of an adult Nile crocodile.

Fig. 1.11. Lateral aspect of the skull of a juvenile Nile crocodile.

thoracic ribs, surrounds the wide cranial aperture of the thorax. This allows large masses to be swallowed. The bones of the forelimb (humerus, radius and ulna) are shorter than their counterparts in the hind limb. The front feet have ve digits, the rst three carrying claws. The pelvic girdle consists of an os ileum, an os ischium directed caudoventrally and an os pubis pointing cranially. The hind limbs are twice as long as the forelimbs, allowing

for a galloping action. Femur, tibia and bula are well developed. The foot has four digits, the rst three carrying claws (Fig. 1.12). The skin Scales and osteoderms Crocodile skin, like that of all reptiles, is covered with scales or scutes and is devoid of sweat glands. On the head the skin is fused

Crocodiles and Alligators

Fig. 1.12. Claws on the left hind foot of an adult Tomistoma schlegelii at Singapore Zoological Gardens (photo P. Martelli).

to the bones of the skull. The large scales on the back, and in some species some of the ventral scales also, contain bony plates, the osteoderms. Muscles connect the ossied dorsal scales with the vertebral column, and when the muscles contract this results in a dorso-ventrally rigid, beam-like structure that allows the crocodile to keep its back and tail straight when walking or running (Frey, 1988a,b). In this context it is interesting to note that recent mitochondrial DNA analyses, as well as studies of nuclear genes, suggested a close relationship between crocodilians and chelonians (tortoises and turtles). The latter also have osteoderms and both dorsal and ventral armour (Hedges and Poling, 1999). Skin glands Crocodilians have a few holocrine skin glands. The cloacal (paracloacal) glands are situated laterally within the lips of the cloaca. The mandibular (gular) glands are in the skin under the tongue, between the mandibles (Fig. 1.13). The septa of the gular glands are lined with melanocytes, giving the gland tissue its black appearance (Weldon and Sampson, 1988). The paracloacal gland is a single secretory sac with a single duct and a single lumen. The

parenchymal cells contain lipid droplets (Weldon and Sampson, 1987). For the analysis of the aromatic secreta of these glands, see p. 52. In some species there are also rudimentary dorsal glands in the Chinese alligator beneath the second row of scales from the dorsal midline, but in various positions from the 2nd to the 15th transverse row (Chen et al., 1991). Identication The patterns of scales, both dorsal and ventral, are species specic, although some slight individual variations may occur. A key for the identication of tanned whole crocodilian skins can be found in Brazaitis (1987). Pigmentation Hatchlings of many species have light and dark transverse striations, which in some species are maintained almost into adulthood. These striations mimic rippling shadows in shallow water (see Fig. 1.3). The chromatophores in the skin can contract and expand following nervous impulses from the eyes via the brain. Blind crocodiles and those kept in complete darkness usually display lighter colours than those exposed to bright daylight.

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Chapter 1

Fig. 1.13. Mandibular (gular) glands of a juvenile Nile crocodile.

The muscles There are no external muscles on the head because the skin adheres to the skull. The powerful jaw muscles are all on the median aspect of the mandible, thus broadening the posterior skull. Sphincters close the external

nares and depressors close the auricular ap over the tympanum for diving. The long dorsal muscles of the trunk extend into the tail. These muscles, plus the ventral tail muscles, musculus (m.) caudofemoralis medially and m. ilioischiocaudalis externally (Frey, 1988a), provide the power for swimming (Fig. 1.14).

Fig. 1.14. Schematic drawing of a cross-section of the tail of a Nile crocodile: 1, musculus (m.) longissimus dorsi; 2, m. caudofemoralis; 3, m. ilioischiocaudalis.

Crocodiles and Alligators

11

The respiratory system Respiratory tract The external nares are slightly raised above the level of the upper jaw, allowing the crocodile to surface and breathe when most of its body is submerged. Adult male gharials develop a large nasal excrescence, the ghara (see Plate 1), which is thought to function as a vocal resonator (Whitaker and Basu, 1983).

In the long nasal passage the olfactory nerve endings are exposed to the air. Except when swallowing, bellowing or yawning, the posterior part of the mouth is closed by the gular valve, consisting of the dorsal ap of the tongue and the palatal ap (velum palati) extending from the soft palate (Putterill and Soley, 1998a) (Fig. 1.15). The Eustachian tubes enter the pharynx in a joined opening just caudally of the internal nares (Colbert, 1946) (Fig. 1.16). Their func-

Fig. 1.15. Schematic drawing of the oral and pharyngeal cavities of the crocodile: 1, gular valve; 2, tongue; 3, larynx and trachea; 4, oesophagus; 5, internal nares; 6, tonsils; 7, Eustachian tubes; 8, nasal passages.

Fig. 1.16. Tonsils of the crocodile caudally of the internal nares.

12

Chapter 1

tion is to equalize the pressure on the two sides of the tympanum (the ear membrane). Close to the opening of the Eustachian tubes into the pharynx there are two mucosal folds, one on either side and extending caudally, which contain tonsillar tissue (Putterill and Soley, 2001) (Fig. 1.16). The glottis has two soft lips (Fig. 1.17) which close when the crocodile swallows. In crocodiles (but not in alligators) the trachea bends to the left inside the thorax before its bifurcation, a substantial distance before entering the lungs (Fig. 1.18). This allows large chunks of prey to be swallowed without exerting any pressure on the trachea or bronchi. Lungs The lungs are multi-cameral sac-like structures, highly vascularized but with thicker walls than a mammalian lung. These thick walls may be necessary to counteract the outside pressure during diving. The lungs lie in pleural chambers which are separated by

a complete mediastinum. The posterior part of the lungs is connected tightly to the anterior transverse membrane (postpulmonary membrane). In crocodiles the remainder of the lungs lies loosely in the thoracic cavity, not as described by Duncker (1989), while in the caiman the lungs are fused to the ventral wall of the thorax. For a detailed study of lung morphology of the Nile crocodile, see Perry (1988). Respiratory muscles The thorax is divided from the abdomen by two transverse membranes. The postpulmonary membrane separates the lungs from the liver, and its ventral third is muscular. The posthepatic (posterior transverse) membrane is attached to a sheet of muscle (m. diaphragmaticus) which extends to the os pubis (Van der Merwe and Kotz, 1993). Together, the two membranes, with their muscular components, act like a diaphragm, pulling the liver in a caudal direction for inspiration.

Fig. 1.17. Tongue and ventral aspect of the pharyngeal cavity with protruding glottis; juvenile Nile crocodile.

Crocodiles and Alligators

13

Fig. 1.18. Tracheal loop in the thorax of Crocodylus palustris.

Voice organ? Crocodiles can produce a range of sounds, but have neither vocal cords (like mammals) nor a syrinx with tympaniform membranes (like birds). It is believed that sounds are produced by forcing the air through the compressed lips of the glottis (Fig. 1.17), much as sounds are produced by human lips in the mouthpiece of a trumpet.

While crocodilian teeth are homomorphic, they may be categorized by their position in the maxilla and mandible. Kieser et al. (1993) group the teeth of the Nile crocodile as follows (Fig. 1.19): maxilla: 5 incisors gap 5 canines gap 5 molars; mandible: 3 incisors gap 5 canines gap 7 molars. The rst mandibular canine is the longest and often extends above the dorsal plane of the snout (Fig. 1.20). This can cause damage to belly skins when frightened young crocodiles pile in the corner of their pen (see also pp. 114 and 241). In some individuals the two mandibular incisors 1 on each side sometimes penetrate the maxilla behind the maxillary incisors and produce openings in the upper lips in front of the nostrils, which could be called false nostrils (Figs 1.9 and 1.21; see also p. 153). Tongue The tongue occupies the oor of the mouth cavity. It is not free but is held in place laterally by a folded membrane. The dorsal surface of the tongue contains mucus glands which are associated with lymphoid tissue,

The digestive system Teeth Crocodilian teeth are pointed, very sharp and are constantly replaced throughout life. The replacement rate varies with the growth rate and slows down as the animal becomes older. In small American alligators (<1.5 m) the estimated replacement rate varied from 3 to 4 months (Erickson, 1996a). Early in life, tooth replacement occurs in waves, passing along alternately numbered tooth series from back to front, while later in life the direction is reversed (Edmund, 1962). Although very old, toothless individuals are sometimes found, this may be due to accumulated damage to the alveoli (Erickson, 1996b) (see p. 247).

14

Chapter 1

Fig. 1.19. Dentition of a juvenile Nile crocodile.

Fig. 1.20. The protruding rst mandibular canine causes scratches when the crocodiles pile up in the corner of their pen.

forming lingual tonsils, while sensory organs are found along the sides of the tongue (Putterill and Soley, 1998b). In crocodiles the dorsal surface also contains salt glands (Taplin and Grigg, 1981; Franklin and Grigg, 1993). Oesophagus The oesophagus extends from the epihyal cartilage of the larynx to the clearly dened gastro-oesophageal junction. It has many longitudinal folds, allowing distension when the crocodile swallows large chunks. The entire epithelial surface contains many

goblet cells that function as an intra-epithelial gland (Putterill et al., 1991). Stomach The stomach lies to the left, immediately behind the left lobe of the liver and the posterior transverse membrane. Its junction with the oesophagus (cardia) is dened by a welldeveloped sphincter muscle. The pyloric exit also lies in the cranial aspect, slightly to the right of the cardia, and is dened by a small bulbus, the pyloric antrum, which in turn opens into the duodenum (Figs 1.221.24). The entire interior surface of the stomach is

Crocodiles and Alligators

15

Fig. 1.21. False nostrils in a captive Crocodylus palustris.

lined uniformly by mucosal glands. Gastrin and somatostatin cells are found only in the glands of the pyloric antrum (Rawdon et al., 1980; Dimaline et al., 1982). The pyloric opening to the duodenum is very small, thus preventing the escape of accidentally swallowed foreign bodies (see p. 254). The gastric wall is strongly muscularized over the fundus, which gives the crocodilian stomach a somewhat gizzard-like appear-

ance. However, the internal glandular lining would not be able to protect the mucosa from a strong chewing action, as the koilin layer does in the avian gizzard. The function of the gastroliths that are often found in crocodilian stomachs, i.e. whether they are ballast, have a chewing function as in birds or have been taken in accidentally, is the subject of an ongoing debate (Steel, 1989) (see also pp. 36 and 290). The fact that stomachs of crocodiles

Fig. 1.22. Overview of the gastrointestinal tract, oesophagus to cloaca, of a Nile crocodile hatchling.

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Chapter 1

Fig. 1.23. Stomach and duodenal antrum of a Nile crocodile. The strong musculature and the central tendinous plate create a gizzard-like impression.

Fig. 1.24. Opened stomach and duodenal antrum of a Nile crocodile. Note the clear demarcation between oesophageal and gastric mucosa.

in the Okawango swamps in Botswana contain increasing amounts of plant material, such as papyrus roots and palm tree seeds, with increasing body length (Blomberg, 1976) tends to indicate accidental ingestion. Intestine The looped duodenum starts from the pyloric antrum and extends to the end of the loop. In many crocodile species the duode-

num folds over again, forming a double loop, although this is apparently not the case in alligators. Both forms occur in different populations of Osteolaemus tetraspis (Huchzermeyer et al., 1995; Huchzermeyer, 1996b). Part of the pancreas is embedded between the limbs of this loop (see Fig. 1.26). From the end of the loop the jejunum runs initially straight along the dorsal aspect of the abdominal cavity, then becomes suspended in loose coils by the mesentery to the

Crocodiles and Alligators

17

point at which the cranial mesenteric artery meets the intestine (van der Merwe and Kotze, 1993). From this point the ileum extends in similar coils to the very short rectum, which in turn enters into the cloaca (Hunter, 1861) (Fig. 1.22). The rectum is suspended by a short mesentery and lies between, and ventral to, the two kidneys. The internal surface of the intestine does not have villi, but a system of complex zigzagging, ridge-like folds, which alternate with each other and are oriented longitudinally (Kotz et al., 1992; Kotz and Soley, 1995) (Fig. 1.25).

Pancreas The proximal (ventral) pancreas lies between the limbs of the duodenal loop, while the distal (dorsal) part surrounds the cranial aspect of the spleen (Miller and Lagios, 1970; Huchzermeyer, 1995) (Fig. 1.26).

Liver The liver lies between the two transverse membranes in the hepatic coelom and has two lobes of almost equal size the right lobe being slightly larger than the left. The

Fig. 1.25. Zigzagging intestinal folds, adult Nile crocodile.

Fig. 1.26. The pancreas between the duodenal loops and extending towards the spleen in a juvenile Nile crocodile.

18

Chapter 1

heart separates these two lobes. In some species the lobes are completely separate, while in others they are joined by a dorsal bridge of liver tissue. Substantial collagenous trabeculae have been found in the liver of American alligators and to a lesser extent in Caiman crocodilus (Beresford, 1992). Storch et al. (1989) found abundant Kupffer cells, as well as fat-storing cells, in the sinusoidal lining of the liver of O. tetraspis. Numerous Kupffer cells are also present in Nile crocodile livers. The gall bladder lies between the two liver lobes within the hepatic coelom, and receives bile from both. The bile duct enters the intestine in the proximal duodenum (Van der Merwe and Kotz, 1993). In most of the American alligators examined by Xu et al. (1997) the right and left hepatic ducts were interconnected, the right duct entering the gall bladder while the left duct continued through the pancreas directly into the duodenum.

gle fold in the African dwarf crocodile and in multiple folds in other crocodile species. These folds continue to grow as the crocodile grows. These multiple folds give the kidney of the Nile crocodile a triangular shape on transverse section, while the kidney of the African dwarf crocodile appears attened. The folding patterns appear to be species specic (Figs 1.271.29). Crocodilians do not have a urinary bladder. The two ureters open into the cloaca. However, urine may be stored in the rectum (Fig. 1.30). The reproductive organs Female Two ovaries are attached to the dorsal body wall cranioventrally to the kidneys, and are partially attached to the cranial part of the kidneys. The ovaries are elongate, and in very young animals they are difcult to differentiate macroscopically from testes. In larger juveniles the follicular structure becomes evident. In adult crocodiles all the follicles mature at the same time (Fig. 1.31). The ovarian histology of the American alligator was studied by Uribe and Guillette (2000). In adult female American alligators the corpora lutea form after ovulation. Their morphology is similar to that in birds and their size can be used to judge whether a female had laid eggs during the preceding season, recent corpora

The urinary system The two kidneys are rmly attached to the dorsal abdominal wall in the most posterior part of the abdomen. As in birds, they are not embedded in perirenal fat and lack a capsule. The renal tissue, consisting of cortical and pelvic layers, is folded over, in a sin-

Fig. 1.27. Kidney of a Nile crocodile.

Crocodiles and Alligators

19

Fig. 1.28. Kidney of Crocodylus palustris.

Fig. 1.29. Kidney of Caiman crocodilus.

lutea having a minimum diameter of 0.4 cm (Guillette et al., 1995b). The ostium of the oviduct lies close to the cranial apex of each ovary. The oviducts are convoluted and increase in size with maturity and sexual activity. They enter the uteri (the glandular part), followed by the vaginae, where the eggs are stored before laying (Fig. 1.32). The vaginae join the cloaca, caudally to the ureters. A small clitoral appendage, which resembles the male penis in shape, is situated ventrally in the cloaca.

Male The slightly attened testes are situated in the same position as the ovaries in the female (Plate 2). A convoluted deferent duct runs along the caudolateral border of each testis and enters the cloaca close to the base of the copulatory organ. This crocodilian penis is folded around a ventral seminal groove (Fig. 1.33). Note that crocodiles and tortoises have only one penis, while lizards and snakes have paired hemipenises.

20

Chapter 1

Fig. 1.30. Rectum lled with urine, juvenile Nile crocodile.

Fig. 1.31. Nile crocodile ovary, with mature follicles.

Crocodiles and Alligators

21

Fig. 1.32. Ovaries, oviducts, uteri and vaginae of Osteolaemus tetraspis.

Fig. 1.33. Everted penis of an adult Nile crocodile.

The endocrine organs Pituitary The pituitary gland lies on the ventral aspect of the brain, at the level of the optic lobes (Fig. 2.26) (Chiasson, 1962).

Thymus The thymus gland consists of a series of lobules of varying sizes on both sides of the trachea along the neck and in the thorax to the base of the heart. In well-nourished crocodiles these glands are embedded in fatty

22

Chapter 1

tissue, which is almost the same colour. This makes it difcult to differentiate the individual lobules. Note that Huchzermeyers (1995) description of the thymus glands of the Nile crocodile was based on emaciated individuals for improved visibility. Consequenly the lobules had vanished from the necks of these animals. However, lobules were subsequently seen in the neck of healthier Nile crocodiles as described previously from other crocodile species (Gegenbauer, 1901; Bockman, 1970). It is believed that in crocodilians the thymus remains active throughout life. For a discussion of the striated muscle cells occasionally found in the reptilian thymus, see Raviola and Raviola (1967). Thyroids While some crocodilians have a single thyroid gland with two well-dened lobes on either side of the trachea, connected by a narrow isthmus (Lynn, 1970), other species have two separate lobes. They are recognized by their dark-brown colour. In the Nile crocodile these are situated not on either side of the trachea, but on the lateral side of each of the two bronchi and medially of the common carotid artery, the right one closer to the entrance of the right bronchus into the lung and the left one closer to the bifurcation of the trachea (Plate 3) (Huchzermeyer, 1995). Parathyroids The two parathyroid glands are normally hidden by thymus tissue and difcult to see. In the Nile crocodile they are situated caudolaterally of the thyroid glands on each side, between the precaval vein and the common carotid artery, immediately cranially of the dorsal bend of the aortic arch (Plate 3 and Fig. 1.35) (Huchzermeyer, 1995). The situation appears to be similar in C. crocodilus, apart from the fact that additional (accessory) parathyroid glands occasionally occur (Oguro and Sasayama, 1976). Adrenals The two adrenal glands are found in the abdominal cavity adhering to the dorsal

body wall. Ventrally they partially overlap the proximal part of the kidneys. They extend cranially beyond the two kidneys and somewhat laterally of the midline (Plate 2) (Huchzermeyer, 1995). Pancreas and intestinal tract The topography of the pancreas has been described above. In the Nile crocodile the islets of Langerhans appear to be present in the distal (dorsal) pancreas only (Huchzermeyer, 1995). A similar distribution was found in the American alligator, in which smaller groups were also found in the ventral (proximal) portion (Jackintell and Lance, 1994). Endocrine cells have also been found in the pyloric part of the stomach and in the intestine of crocodiles (Rawdon et al., 1980; Dimaline et al., 1982; van Aswegen et al., 1992).

The circulatory system and blood cells Heart In the Nile crocodile the heart is situated between the 4th and 8th thoracic ribs (Van der Merwe and Kotz, 1993) and between the two lobes of the liver (Fig. 1.34). The situation is similar in the other crocodilians. A ligament at its apex, the gubernaculum cordis (Webb, 1979), connects it to the pericardial sac and beyond this to the postpulmonary transverse membrane. There is no fat in the coronary groove. The two auricles stretch caudally on either side halfway along the ventricles, the larger right auricle sometimes further. The four chambers are completely separated. Circulation The major blood vessels leaving the heart of the Nile crocodile are identied in Fig. 1.35. Crocodiles have two aortic arches like other reptiles. The left aortic arch leaves the right ventricle alongside the pulmonary artery and becomes the coeliac artery; this supplies the digestive organs of the abdomen. The

Crocodiles and Alligators

23

Fig. 1.34. The heart is situated between the lungs and the two lobes of the liver; juvenile Nile crocodile.

Fig. 1.35. Schematic drawing of the heart and major blood vessels of the Nile crocodile, ventral aspect. 1, trachea; 2, thyroid; 3, carotid artery; 4, precaval vein; 5, parathyroid; 6, aortic arch; 7, left auricle; 8, left ventricle; 9, bifurcation of the trachea; 10, carotid artery; 11, thyroid; 12, precaval vein; 13, parathyroid; 14, aortic arch; 15, right auricle; 16, right ventricle.

right aortic arch emerges from the left ventricle and runs posteriorly as the dorsal aorta. The left and right aortic arches communicate in two places: the foramen of Panizza and the anastomosis (Axelsson and Franklin,

1997). The foramen of Panizza is located at the base of the heart within the aortic arch valves (Webb, 1979), and the anastomosis is a short vessel connecting the two aortic arches. In American alligators of length 12 m, the foramen of Panizza had a diameter of

24

Chapter 1

12 mm (Greeneld and Morrow, 1961). During systole it is completely covered by the aortic valves, thus allowing an exchange of blood during diastole only (Axelsson and Franklin, 1997). As in all reptiles and birds, part of the venous blood of the caudal half of the body is drained through the renal portal system. According to Chiasson (1962) this appears to be bypassed partially by the ventral abdominal veins which, together with the mesenteric vein, enter the hepatic portal system. Supercial veins I have been unable to identify any large, easily accessible supercial veins for intravenous injections. Blood can be drawn from the dorsal and ventral vertebral veins of the neck and tail (see p. 64). The statement about drawing blood from the temporal vein, which lies just below the temporal muscle on the dorsal aspect of the head (Lance, quoted by Samour et al., 1984), is in error. Such a technique has never been used or described by Lance (personal communication, V.A. Lance, San Diego, 1999). Tonsils In the Nile crocodile the tonsils are situated in the roof of the pharynx (Putterill and Soley, 2001) (see above, Fig. 1.16). Spleen The pear-shaped spleen lies dorsally in the mesentery, close to the base of the duodenal loop (Plate 2). Its broad cranial end is embedded in the caudal limb of the pancreas. The spleen is covered by a strong capsule. The histology and vascular architecture of the spleen of the American alligator were studied by Tanaka and Elsey (1997). Lymphatics The lymphatic system was studied by McCauley (1956). There are no subcutaneous lymph vessels and no lymph nodes. Lymph vessels from the head and the anterior limbs, thorax and abdomen anastomose with the

external jugular vein just proximal to the juncture with the subclavian vein. The lymph from the caudal and pelvic regions is pumped by the posterior lymph hearts into small vessels which empty into the pelvic venous plexus. These lymph hearts are single-chambered muscular structures, measuring 3 57 mm in alligators 5075 cm long. They are situated supercially at the junction of the hind limb with the pelvis, below the supercial layer of the deep fascia in the triangle formed by the m. longissimus caudae, the crest of the ileum and the m. exor caudae. In the absence of lymph nodes, the thymus (see above), tonsils, spleen and numerous lymphoid masses in the walls of the digestive tract act as reservoirs of lymphocytes. Blood volume The total blood volume of one juvenile American alligator was 4.2% of body mass (Coulson et al., 1950), of another two alligators 5.1% and 5.5% (Andersen, 1961), and that of 3.5-year-old Cuban crocodiles (n = 19) was 4.0 0.3% for males and 3.6 0.2% for females (Carmena-Suero et al., 1979). Blood cells All crocodilian blood cells are nucleated. The erythrocytes are oval in shape with round or oval nuclei. The dimensions of the red blood cells of some crocodilian species are given in Table 1.1. The following descriptions of the various blood cells were taken from Mateo et al. (1984b) and refer to the American alligator. Detailed descriptions of the blood cells of Crocodylus porosus and Crocodylus johnsoni are given by Caneld (1985). See also Hawkey and Dennett (1989). However, there is some confusion in the literature, with different authors using different denitions for the different leucocytes.
THROMBOCYTES. Length 14.3 m, oval or elliptical with smooth cell borders, smooth pale blue or almost colourless cytoplasm that often contains numerous clear conuent

Crocodiles and Alligators

25

Table 1.1. Erythrocyte dimensions (means). Species Alligator mississippiensis A. mississippiensis A. mississippiensis A. mississippiensis Caiman latirostris C. latirostris Caiman crocodilus A. mississippiensis C. latirostris C. crocodilus Length ( m) 14.822.0 17.5 23.2 23.0 21.3 19.5 23.8 20.8 17.0 17.0 Width ( m) 8.112.8 9.7 12.1 14.3 10.9 10.8 13.3 11.1 9.0 9.0 References 1 4 5 6 2 2 3 3 7 7

1, Reese (1917); 2, Gulliver (1840) (cited by Reese, 1917); 3, Milne-Edwards (1856) (cited by Reese, 1917); 4, Glassman et al. (1981); 5, Wintrobe (1933); 6, Mateo et al. (1984); 7, Troiano et al. (1998). Note the nomenclature used in the older papers: Alligator lucius = Alligator mississippiensis; Alligator sclerops = Caiman crocodilus; Caiman ssipes = Caiman latirostris.

vacuoles with poorly demarcated borders. The uniform oval nuclei are located centrally and oriented longitudinally, staining intensely dark purple, with coarsely condensed chromatin. A phagocytic function of avian thrombocytes was discovered recently (Wigley et al., 1999) and the same function may be postulated for reptilian thrombocytes. The functions of the other blood cells are presumed to be the same as in mammals and birds.
HETEROPHILS.

nent coarsely clumped chromatin and very sharply demarcated borders, usually located at one pole of the cell, often causing a slight outward bulge of the cell outline. Some nuclei are located more centrally. The paleblue, smooth cytoplasm is visible only as a thin rim surrounding the many bright pink plump granules measuring 23 m (Fig. 1.37). Often a few granules are present on the face of the nucleus.
BASOPHILS. Basophils, or type III granulocytes (Caneld, 1985), are round cells with irregular external cobblestone contours and a diameter of 12.8 m. Abundant, dark-purple to purplish-red, round granules measuring 0.10.5 m pack the cell to the point where they frequently obscure the nucleus. Sometimes the granules are arranged in a peripheral rim with a central cluster over the nucleus. LYMPHOCYTES.

Heterophils, or type I granulocytes (Caneld, 1985), are round to oval cells with mean diameters of 17.3 m and distinct smooth cytoplasmic borders. The nuclei are lenticular, oval or, rarely, bilobed, with indistinctly clumped purple chromatin, usually eccentrically located at one pole of the cell. The cytoplasm contains abundant, 34 m long, fusiform refractile granules, occasionally arranged in perinuclear radially symmetrical star-like congurations (Fig. 1.36).

EOSINOPHILS. Eosinophils, or type II granulocytes (Caneld, 1985), are oval or occasionally round, with a mean diameter of 14.9 m and smooth cytoplasmic outlines. The lenticular or oval nuclei are purple with promi-

Lymphocytes are generally round or oval, with a diameter of 10.7 m, but irregular, polygonal forms are also seen. A large nucleus, with smooth outlines and following the cell contours, almost lls the cell. The nucleus is pale violet with nely clumped chromatin. The cytoplasm is visible only as a thin, slate-grey or pale-blue rim

26

Chapter 1

Fig. 1.36. Heterophil (h) of a Nile crocodile.

Fig. 1.37. Two eosinophils, Nile crocodile.

bordering the nucleus. Occasionally dustlike red granules and/or a few clear vacuoles, 1 m in diameter, are scattered through the cytoplasm. External cell borders range from smooth to ragged, frequently with bleb-like protrusions of cytoplasm.
MONOCYTES. Monocytes are oval or round with a diameter of 14.3 m, with somewhat

indistinct external cell borders and numerous delicate cytoplasmic projections. The abundant grey-blue cytoplasm sometimes contains a few clear, refractile vacuoles, measuring 1.2 m. Many cells have ne dust-like granules, usually arranged in crescentic perinuclear aggregates. The plump, oval nucleus, measuring 7.1 m, is usually located centrally, but is sometimes eccentri-

Crocodiles and Alligators

27

cally situated adjacent to one pole of the cell. The nucleus is homogeneous light purple with nely stippled chromatin (Fig. 1.38). In addition to these typical monocytes, large cells, up to 20 m in diameter, with undulating borders, pale-blue cytoplasm with few inclusions, and prominent, indented or even horseshoe-shaped nuclei are seen occasionally. Details of crocodilian haematology are given in Chapter 2. Chromosomes The chromosomes of 21 species of crocodilians were studied by Cohen and Gans (1970) and of ve species and several crossings by Chavananikul et al. (1994). The number of chromosomes ranges from 30 to 42 and the fundamental number from 56 to 62, for details see Table 1.2. There are no sex chromosomes.

between the hemispheres and the relatively small cerebellum. The base is formed by a relatively broad medulla oblongata. Spinal cord The spinal cord extends almost to the tip of the tail. There is no cauda equina, as each pair of caudal nerves leaves the cord at the site of exit from the vertebral column (Chiasson, 1962). Peripheral nerves The peripheral nerves exit the spinal cord in pairs. At the level of the pectoral and pelvic girdles they are organized into a brachial and lumbo-sacral plexus, respectively. For a detailed description see Chiasson (1962). Autonomic nervous system Like higher vertebrates, crocodiles also have an autonomous nervous system, consisting of two components. The vagus nerve starts as the tenth cranial nerve and runs along the jugular to the thoracic and abdominal viscera. The sympathetic trunk runs parallel to the spinal cord and communicates with each spinal nerve, thickening at each site of communication in the form of a sympathetic ganglion (Chiasson, 1962).

The nervous system and sensory organs Brain The most striking features of the crocodilian brain are the two olfactory bulbs, which extend anteriorly far beyond the two cerebral hemispheres. The optic lobes are exposed

Fig. 1.38. Monocyte (m) of a Nile crocodile.

28

Chapter 1

Table 1.2. The chromosomes of crocodiles. Cohen and Gans (1970) Species Palaeosuchus trigonatus P. palpebrosus Melanosuchus niger Caiman latirostris C. crocodilus Alligator mississippiensis A. sinensis Gavialis gangeticus Crocodylus siamensis C. porosus C. moreletii C. johnsoni C. acutus C. intermedius C. niloticus C. novaeguineae C. cataphractus C. rhombifer C. palustris Osteolaemus tetraspis Tomistoma schlegelii 2n 42 42 42 42 42 32 32 32 34 34 32 32 32 32 32 32 30 30 30 38 32 NF 58 58 60 60 62 60 60 60 58 58 56 58 58 58 58 58 58 58 58 58 58 Chavananikul et al. (1994) 2n NF Amavet et al. (2000) 2n

42 42

30 34

58 58

32 32 30

58 58 58

2n, Diploid number; NF, fundamental number.

Ear The ear has two sensory functions, hearing and spatial orientation.
HEARING.

The tympanic membrane of the ear is protected by a brous ap which closes when diving. In the middle ear the columella is attached to the tympanic membrane and at the other end it has a large basal plate set in the fenestra ovalis of the inner ear.

which is optically clear and protects the cornea during diving. A special muscle can retract the eye into the orbital fossa. A reecting layer behind the retina improves night vision and causes crocodile eyes to light up at night in the beam of a torch (Fig. 1.39). There is no night vision in complete darkness without a minimum of residual light. Fat storage Fat body Being exothermic, crocodiles do not need fat for insulation. In fact, subcutaneous fat deposits would impede thermoregulation (see p. 44). Also, crocodiles do not store fat in the coronary groove of the heart. In mammals, there is growing evidence that the heart uses mainly fat as a source of energy (Medeiros and Wildman, 1997). It is believed that this is also the case in crocodiles, and that the fat supply for the heart is stored in the abdominal fat body, for which I propose the anatomical name the steatotheca (Greek stear = fat;

SPATIAL ORIENTATION. The membranous labyrinth consists of three semicircular canals, each with an ampulla, the utriculus and its ventral extension, the lagena, all enclosed in bone.

Both functions are served by the acoustic nerve (eighth cranial nerve) (Chiasson, 1962). Eye The eye is protected by three eyelids. The third eyelid is the nictitating membrane,

Crocodiles and Alligators

29

Fig. 1.39. Light of the photographic ash reected by the eyes of the juvenile Nile crocodiles on a farm in South Africa (photo A. Brieger).

th\k\ = container, store). This organ is located in a mesenteric fold close to the right abdominal wall, immediately posterior to the liver (Fig. 1.40) (Vorstman, 1939; Mushonga and Horowitz, 1996). Its volume varies with the state of nutrition, while its shape varies from species to species (Fig. 1.41). The fat cells have large nuclei, demonstrating their ability to activate the stored fat rapidly (Fig. 1.42).

Somatic fat Additional fat may be stored in somatic fat cells with small nuclei: in the mediastinum of the thorax, under the peritoneum and between muscles, particularly ventrally in the tail between the inner (caudofemoralis) and external (ilioischiocaudalis) muscles.

Fig. 1.40. The abdominal fat body of a juvenile Nile crocodile, caudally of the right lobe of the liver and partially hidden by the duodenal loop.

30

Chapter 1

Fig. 1.41. Abdominal fat body of Osteolaemus tetraspis.

Fig. 1.42. Histology of an almost depleted abdominal fat body of a Nile crocodile hatchling. Note the large nuclei of the fat cells.

The egg Crocodilian eggs are elongate elliptical and have a hard shell. The size of the egg varies with the species, with the age of the female that lays the egg young females laying smaller eggs than mature females and indi-

vidually between females. Larger eggs produce stronger and more viable hatchlings, which rapidly outgrow hatchlings from smaller eggs. Parameters of American alligator eggs were determined by Cardeilhac et al. (1999b) and are summarized in Table 1.3.

Crocodiles and Alligators

31

Table 1.3. Summary of mean parameters of eggs of three different populations of American alligators (after Cardeilhac et al., 1999b). Parameter Egg length (cm) Egg width (cm) Egg mass (g) Length/width ratio Shell thickness (mm) Shell density Shell mass (g) Shell mass (% of egg mass) Yolk mass (g) Yolk mass (% of egg mass) Membrane mass (% of egg mass) Result 7.257.57 4.0794.47 68.8586.0 1.6841.766 0.430.45 2.102.14 7.398.89 10.5711.14 31.936.2 4448 1.061.08

Eggshell The calcareous shell consists of an outer, densely calcied layer, in which the calcite crystals are stacked vertically; a honeycomb layer of horizontally stacked crystals; an organic layer, which contains a higher percentage of organic matrix; and a mammillary layer. Pores penetrate the shell surface and end between the mammillae. These pores are most frequent in the opaque zone (Ferguson, 1982). A thin, organic, probably mucinous, layer was found to cover the outer surface of some newly laid eggs and was believed to consist of the remnants of oviductal secretions. This layer was no longer present after 2 weeks of incubation. It is therefore not an equivalent

of the wax cuticle present on most avian eggs (Ferguson, 1982). Under the calcareous shell lies the eggshell membrane, consisting of two layers, a brous membrane facing the shell and a limiting membrane facing the embryo. The limiting membrane contains a large number of tiny pores and fewer large pores. Most of these pores are closed at the onset of incubation and others open up as incubation proceeds. Consequently, the shell membrane is less permeable to oxygen than the calcareous shell (Kern and Ferguson, 1997). The opaque band around the lesser circumference of the egg develops during incubation in parallel with the expansion of the chorioallantoic membrane and the mobilization of calcium out of the shell for use by the embryo (Fig. 1.43). At the same time, an extrinsic acidic degradation of the outer shell occurs due to microbial action in the nest. This produces erosion craters around the pores and increases the permeability of the shell (Ferguson, 1982). Unlike the avian egg, the crocodile egg does not have an air chamber between the shell and the shell membrane (Ferguson, 1982). Internal components The yolk, with the embryonic disc oating on top, is surrounded by a large quantity of thin albumen, which in turn is contained in a

Fig. 1.43. A banded Nile crocodile egg after removal of its contents.

32

Chapter 1

layer of thick albumen separating it from the shell (Magnusson and Taylor, 1980). If the egg is turned during laying, gravity causes the yolk with the embryo to rotate. Within 24 h of laying, the developing vitelline membrane and the embryo adhere to the shell membrane, displacing the albumen towards the poles of the egg (Webb et al., 1987). The embryo From the start of embryonic development in the oviduct, water is drawn from the albumen and secreted beneath the embryo on the inside of the vitelline membrane, where it forms the subembryonic uid. After laying, the volume of subembryonic uid increases rapidly, causing the volume within the vitelline membrane (containing embryo, subembryonic uid and yolk) to expand (Webb et al., 1987). Albumen dehydration and the production of subembryonic uid peak at the time of the expansion of the allantois. Along the shell the allantois fuses with the chorion and forms the chorioallantois (Webb et al., 1987), which becomes highly vascularized and takes on the gas-exchange function until hatching, when the lungs are able to ll with air. The different embryonic membranes and spaces are shown schematically in Fig. 1.44.

Crocodilian Physiology
Yolk-sac resorption Just before hatching, the yolk-sac is drawn into the abdominal cavity and the body wall closes around the navel. At this point gas exchange can no longer take place via the membranes and the young pre-hatchling has to start using its lungs. The yolk-sac has already provided nutrition during embryonic and fetal development, and (in American alligators) has lost 25% of its mass (Fischer et al., 1991), but still contains sufcient nutrients (75% of its contents in American alligators) for the rst few weeks, until the hatchling is strong enough to nd its own food (Fischer et al., 1991). The contents of the yolk-sac are resorbed in two distinct ways: (i) direct resorption into the bloodstream via a capillary bed which has developed in the wall of the yolk-sac; and (ii) voiding via the vitello-intestinal duct into the intestine, digestion there and nally resorption through the intestinal mucosa. The open vitello-intestinal duct is also a major pathway for infection of the yolk-sac with intestinal bacteria, depending on intestinal colonization and peristaltic movements (see p. 142). The vitelline duct connecting the yolk-sac to the intestine is shown

Fig. 1.44. Schematic drawing of a crocodile embryo and its membranes at 45 days of incubation; ca, chorioallantois; m, shell membrane; s, shell; y, yolk-sac (after Webb et al., 1987).

Crocodiles and Alligators

33

in Fig. 1.45. Unlike the situation in birds, the crocodilian yolk-sac does not appear to be anchored to the navel. There do not appear to be any reports about the time it takes for the yolk-sac to be completely resorbed under normal circumstances. It is probably 34 weeks. This would be temperature dependent, with a slower rate of resorption at lower (suboptimal) temperatures. Infection of the vitello-intestinal duct can lead to its closure and, in this case, the yolk-sac will remain unresorbed (see p. 143). Sex differentiation Crocodiles do not have sex chromosomes (see above). Instead, the sex of the embryo is determined by the incubation temperature. Recently, Crews and Ross (1998) reviewed current knowledge about the mechanisms involved, as follows. At the temperature-sensitive stage early in embryonic development, temperature inuences the expression of stereogenic factor 1, which in turn upregulates the expression of the gene for aromatase, the critical

enzyme in the synthesis of oestrogen. Oestrogen then binds to the oestrogen receptor, the expression of which is also modulated by the incubation temperature. Via this cascade of events low incubation temperatures favour the development of ovaries, while at high temperatures testes are produced. However, this cascade can easily be inuenced, or even disrupted, by the action of external steroids (see p. 223).

Growth Factors inuencing growth The growth of juvenile crocodiles depends mainly on the environmental temperature conditions and on nutrition, although genetic and clutch-related factors probably also play a role (Garnett and Murray, 1986). The most important clutch-related factor is egg size and consequently hatchling size, as small hatchlings are generally poor growers. Stress caused by high stocking density can depress the growth rate (Elsey et al., 1990a) (see also pp. 116 and 280).

Fig. 1.45. One-day-old gharial hatchling, showing the yolk-sac connected to the intestines by the vitelline duct. Note the double duodenal loop of this species.

34

Chapter 1

Metabolic rate The metabolic rate of crocodiles depends on their size and activity, and the temperature (Baldwin et al., 1995; Munns et al., 1998). At 28C a 70 kg American alligator produces about 72 kcal day 1, i.e. about 4% of that of a person of equal mass. At 32C the rate doubles. However, a hatchling at 28C has half the human metabolic rate (Coulson et al., 1989). Stress-related reduction of the growth rate runting of some individuals is a common occurrence on crocodile farms (see p. 234). A positive inuence of sunlight on the growth rate was found by Zilber et al. (1991), but the small number of individuals involved, the poor overall growth rates achieved and the high mortality in the experimental groups severely limit the usefulness and credibility of their results. Generally, growth rates, particularly weights, achieved on farms exceed those in the wild. One-year-old wild IndoPacic crocodiles attained 0.73 m and 0.87 kg, while farmed ones of the same age averaged 0.75 m and 1.36 kg (Webb et al., 1991). Crocodiles may continue growing throughout their life, males faster than females. The growth of adult females is further reduced by reproductive demands. With increasing age the growth in length slows down and is replaced by growth in width, leading to a maximum length, at least in American alligators, which might not be exceeded (Woodward et al., 1995). Young females lay smaller eggs and smaller clutches than older ones. There is also some indication that, in individual females, egg size and clutch size are inversely related.

The correlation between myocardial mass, i.e. the mass of the two ventricles of the heart, and body length of Nile crocodiles was examined by Huchzermeyer (1994). The ventricular mass can be used as a standard for the evaluation of other more variable organs, particularly the fat body and spleen (see p. 85). Bone rings In most crocodilian species growth is seasonal and this is reected by bone deposition. Such growth rings can be detected histologically and are used to estimate the age of the crocodile in question (de Buffrnil, 1980a,b; de Buffrnil and Buffetaud, 1981; Wagner et al., 1990). Experimentally, this method can be enhanced by feeding tetracycline which is deposited in the bone in the form of visible, stained rings (Roberts et al., 1988). The growth rate of crocodilians is limited by the slow deposition of lamellar bone. This was the case even in the giant crocodile Deinosuchus of the Late Cretaceous period of North America (up to 10 m in length), which is estimated to have taken 35 years to reach adult size (Erickson and Brochu, 1999). Agelengthweight relations The agelength relation depends on the growth rate, while the lengthweight relation depends on the actual state of nutrition. Consequently these relations differ between wild and farmed crocodiles, the latter growing faster and being fatter. There are also individual differences. Some examples of such relations in American alligators, Nile crocodiles and African dwarf crocodiles are given in Tables 1.4 to 1.6. Further lengthweight relations for Nile crocodiles can be found in Table 2.10. Mathematical approaches to lengthmass relationships of crocodilians were explored by Wilkinson et al. (1997). Longevity While captive American alligators may live for up to 70 years, they do not appear to

Allometry Allometric studies have shown that the body and tail grow faster than the head and legs, although at some stage the snout length grows faster than any other part measured. These changes in the proportions of the different parts of the body allow the growing crocodiles to adjust to the different demands made by the environment on crocodiles of different sizes (Kramer and Medem, 1955; Junprasert and Youngprapakorn, 1994).

Crocodiles and Alligators

35

Table 1.4. Agelengthweight relations of marked and released American alligators (McIlhenny, 1934). Age 1 day 32 days 10 months 12 months 15 months 20 months 21 months 2 years 1 month 2 years 8 months 3 years 2 months 3 years 10 months 4 years 2 months 6 years 6 years 9 years 9 years 10 years 10 years 11 years Sex Length (m) 0.230.24 0.340.37 0.45 0.67 0.690.81 0.75 0.790.82 0.991.20 1.091.14 1.271.50 1.181.73 1.581.71 1.611.75 1.752.39 2.012.08 2.352.68 2.172.21 2.692.87 2.643.07 Weight (kg) 0.0710.085 0.24 1.84 1.932.37 1.41 1.641.84 4.355.64 3.664.54 7.839.57 5.0613.3 8.8517.5 13.617.3 18.956.6 38.240.4 57.067.6 49.952.8 80.7132.2 76.9160.6

Female Male Female Male Female Male Male

Table 1.5. Agelengthweight relations in farmed Nile crocodiles (Loveridge and Blake, 1972). Age 1920 months 32 months 3233 months 4647 months 5154 months Sex Female Male Female Female Female Female Male N 5 4 4 2 2 2 1 Length (m) 0.911.18 1.181.33 0.981.40 1.181.75 1.91 2.82 3.92 Weight (kg) 1.755.3 5.58.9 3.29.7 5.925.4 32.633.5 125 312

Table 1.6. Agelengthweight relations of two African dwarf crocodiles reared in captivity (Helfenberger, 1982). Age 10 weeks 6 months 1 year 2 years Length (m) 0.260.31 0.360.41 0.63 0.770.78 Weight (kg) 0.080.14 0.230.40 1.291.40 2.012.70

Locomotion Swimming The crocodilian body is designed primarily for swimming. During this action the front legs are held parallel to the thorax, while the hind legs are partially spread out to act as rudders. Sideways movements of the tail provide the propelling force for both slow and rapid swimming. Rapid swimming can be extremely fast and can catapult the crocodile out of the water at a very high speed when it attacks a prey on land close to the water. At lower temperatures the swimming speed is reduced. In juvenile American alligators the swimming speed increased at

reach more than 50 years in the wild (Woodward et al., 1995). Similar ages may be attained by individuals of other crocodilian species. However, estimates may be far out. An American crocodile with an estimated age of 100 years was mentioned by Jasmin and Baucom (1967).

36

Chapter 1

temperatures from 15C to 20C, but not between 20C and 30C (Gatten et al., 1991). Sliding Sliding occurs when the body is not lifted off the ground. This kind of motion is used over short distances on land and always when going into water. Sometimes referred to as sprawling, it is also seen in the transition from stationary to high walk (Elias and Reilley, 1996). On farms sliding can damage the chin, the belly skin and the soles of the feet if the oor of the pen consists of concrete that is not absolutely smooth or covered with a protective paint. Gharials cannot walk. On land they slide, moving their body forward with all four legs acting simultaneously. Walking When walking the crocodile lifts its whole body off the ground. In this way it can move over rough terrain without getting scratched or torn. It is a stately motion, similar to that of a tortoise when walking. It is also referred to as high walk. Running A faster way of moving on land is running, which is a kind of galloping motion. This can be quite fast, but can only be sustained over short distances. Jumping Hatchlings and yearlings of the African dwarf crocodile have an additional mode of locomotion. They use their relatively strong hind legs to jump in a frog-like fashion when frightened while on land. Each jump propels the hatchling forward by up to 1 m and it may jump several times in succession. Crocodiles can also jump out of deep water to catch prey high above the water or out on land. To achieve this they gather speed under water before surfacing.

Digestion Ingestion Small prey is swallowed whole, though it is at least punctured during the act of catching and killing. Larger prey is masticated for a while before deglutination (Diefenbach, 1975a). However, crocodiles do not reduce the size of the morsels by prolonged chewing. Excessively large prey is reduced by worrying and ripping off bits or limbs by rapid rotation around the longitudinal axis of the crocodile. Ripping is facilitated when several crocodiles feed from the same carcass. Small bits are taken off the ground by holding the head sideways (see Fig. 3.20). Reduction In the stomach the swallowed food is exposed to the action of hydrochloric acid (HCl) and peptic proteolysis. Their secretion is stimulated by the presence of the food, while penetration into the food is facilitated by the puncturing and chewing that has taken place before swallowing. Gastric pH drops as low as 1.2 and in fasting animals even stays below 2.5 (Diefenbach, 1975a). Gastric contractions mixing the stomach contents take place 23 times per minute when the stomach is full (Diefenbach, 1975b). At 30C complete emptying of the stomach took 99 h on average and at 15C 315 h (Diefenbach, 1975b). However, Kanui et al. (1991) recorded gastrointestinal passage times in 12-week-old Nile crocodiles as 35 h at 30C and 44 h at 25C. Lithophagy Stones (gastroliths) are often found among crocodilian stomach contents. The question remains whether these stones are needed to grind the ingested food, similar to the situation in an avian gizzard, whether they are needed as ballast, or whether they are swallowed accidentally (Sokol, 1971) (see also p. 15). Here it should be noted that predatory (carnivorous) birds do not use stones in their gizzards. Fitch-Snyder and Lance (1993)

Crocodiles and Alligators

37

observed captive juvenile American alligators actively seeking out and swallowing gravel. However, this could have been due to a behavioural disturbance similar to the frequently seen ingestion of foreign objects by stressed farmed or captive ostriches (Huchzermeyer, 1996a) (see also pp. 281 and 290). Regurgitation When American alligators eat hairy prey, the indigestible hair forms hair balls, which are then regurgitated. Smaller foreign bodies may also become incorporated in these hair balls and regurgitated as well. Even radio collars attached to released juvenile alligators have been found regurgitated after the bearers had been cannibalized (Chabreck, 1996; Chabreck et al., 1996). Digestion The combined action of pepsin and HCl in the stomach digests most of the protein in the food and dissolves the bones of the prey. Further protein, glycogen and fats are digested in the upper small intestine under the action of bile and pancreatic secretions. There is some evidence that frequent lling of the stomach reduces the digestive efciency of the system (Webb et al., 1991). There is a suspicion that excess fat in the diet might interfere with proteolytic activity and therefore Webb et al. (1991) recommend a maximum of 9% fat in crocodile rations. Assimilation Assimilation is the uptake of the digested food from the intestine either into the venous circulation and hence into the liver, or via the lymph directly into the general circulation. This takes place throughout the length of the small intestine (duodenum, jejunum and ileum). Seasonal suppression of appetite Coulson et al. (1950) observed that captive American alligators practically stopped feeding during autumn and winter, although

they were kept at a constant temperature. It is unclear whether this response was triggered by diminishing daylength or whether it might be governed by a built-in body clock. This phenomenon has also been observed in captive Nile crocodiles (personal communication, L. Fougeirol, Pierrelatte, 2002). Normal oral ora Identication of the oral ora of crocodilians is important for the treatment of bite wounds. The work done on American alligators can be taken as representative for all crocodilian species. Doering et al. (1971) isolated Clostridium spp., Citrobacter, Enterococcus spp. and others from two American alligators. Flandry et al. (1989) examined ten alligators from three different locations and found both aerobic and anaerobic bacteria in all of them, but isolated fungi from only seven individuals (Tables 1.71.9). The bacterial oral ora of 19 farmed spectacled caimans in Brazil comprised the genera Citrobacter, Providencia, Escherichia, Proteus, Morganella, Serratia, Edwardsiella, Aeromonas, Acinetobacter, Staphylococcus, Streptococcus and Bacillus (Matushima and Ramos, 1993).
Table 1.7. Oral anaerobic bacterial ora of ten American alligators (Flandry et al., 1989). Genus Bacteroides Species asaccharolyticus bivius loeschei/denticola oralis sordellii thetaiotamicron vulgatus bifermentans clostridioforme limosum sordellii tetani nucleatum varium magnus prevotii N 2 3 2 3 1 1 1 3 1 1 2 1 2 3 1 3

Clostridium

Fusobacterium Peptococcus

N, number of isolates.

38

Chapter 1

Table 1.8. Oral aerobic bacterial ora of ten American alligators (Flandry et al., 1989). Genus Acinetobacter Aerobacter Aeromonas Citrobacter Corynebacterium Diphtheroides Enterobacter Klebsiella Moraxella Morganella Pasteurella Proteus Pseudomonas Species calcoaceticus var. wolf radiobacter hydrophila freundii sp. sp. cloacae oxytoca sp. morganii haemolytica sp. vulgaris cepacia uorescens pickettii odorifera N 1 3 9 4 1 2 2 1 1 1 1 1 7 2 1 1 1

Flora of the gular and paracloacal glands Williams et al. (1990) isolated the following aquatic and intestinal bacteria from either or both pairs of the exocrine skin glands of 23 adult American alligators: Acinetobacter anitratus, A. wolf, Aeromonas hydrophila, Bacillus sp., Citrobacter amalonaticus, C. freundii, Corynebacterium sp., Enterobacter agglomerans, E. cloacae, Edwardsiella tarda, Escherichia coli, E. hermanii, Flavobacterium indoltheticum, F. gleum, F. multivorum, Hafnia alvei, Klebsiella pneumoniae, Proteus mirabilis, Pseudomonas cepacia, P. maltophila, Serratia marcescens and Yersinia enterocolitica.

Normal intestinal ora The intestinal ora plays an important protective role by occupying the available attachment sites and thereby displacing pathogenic intruders, a phenomenon referred to as competitive exclusion. Intensively reared crocodiles often have a single-species ora, an abnormal situation that makes them prone to intestinal infection. Despite its importance, this appears to be a neglected subject, probably partly due to the difculty of obtaining specimens from animals in the wild, since they are usually in remote places. Most of the published results are from captive crocodiles and it is doubtful that they are representative of a normal intestinal ora. Campylobacter fetus subspecies jejuni serotype 23 was isolated from a captive African dwarf crocodile (Luechtefeld et al., 1981). Misra et al. (1993) examined cloacal swabs of 23 captive gharials and the results are shown in Table 1.10.
Table 1.10. Aerobic bacterial intestinal ora of captive gharials, N = 23 (Misra et al., 1993). Organism Pure 4 1 3 1 2 Mixed 10 6 6 7

Serratia

N, number of isolates.

Table 1.9. Oral fungal ora of ten American alligators (Flandry et al., 1989). Genus Aspergillus Candida Species avipes humicola lipolytica rugosa zeylansides sp. sp. sp. sp. sp. sp. sp. rubra sp. beigelii sp. N 1 1 1 2 1 1 1 1 1 2 1 1 2 2 2 1 6

Cladosporium Curvularia Drechsleria Epicoccum Fusarium Penicillium Rhodotorula Trichoderma Trichosporon Torulopsis Unidentied moulds

N, number of isolates.

Crocodiles, particularly in captive or farm situations, tend to contaminate their aquatic environment with faecal bacteria and fungi. Thus it is not surprising that the oral ora should be similar to that of the intestine.

Staphylococcus sp. Aeromonas hydrophila Citrobacter sp. Edwardsiella tarda Haffnia alvei Escherichia coli

Crocodiles and Alligators

39

Roggendorf and Mller (1976) isolated Citrobacter sp., Escherichia coli, Proteus mirabilis, P. vulgaris and Aeromonas hydrophila from the faeces of one captive Nile crocodile and Citrobacter sp., Providentia rettgeri and Aeromonas hydrophila from the faeces of a C. crocodilus. Huchzermeyer and Agnagna (1994) reported the isolation of aerobic bacteria and fungi from 21 wild-caught and severely stressed African dwarf crocodiles which were sampled when they were slaughtered at markets in Brazzaville, Congo Republic. These and subsequently published isolations from samples collected during a second expedition in 1995 (Huchzermeyer

et al., 1999) are shown in Tables 1.11 and 1.12. Respiration Ventilation There are two types of ventilatory movements, pharyngeal and thoraco-abdominal. Pharyngeal ventilation does not contribute to the air ow to the lung. It only serves to move air through the nasal passages for olfaction. Thoraco-abdominal movements involve the diaphragmatic muscles for inhalation and the intercostal and abdominal muscles for exhalation (Gans and Clark, 1976).

Table 1.11. Aerobic bacterial intestinal ora of African dwarf crocodiles (Huchzermeyer et al., 2000). Genus Alcaligenes Bacillus Species faecalis alvei cereus circulans coagulans amalonaticus freundii nishinomyaensis agglomerans cloacae gergoviae caecorum durans faecalis faecium pseudoavium solitarius coli balustinum odoratum oxytoca varians gibsonii sp. luteus mirabilis serovars odorifera chromogenes epidermidis xylosus salivarius sp. N (1993) N (1995) 2 1 4

Citrobacter Dermacoccus Enterobacter

11 1 1 1 3 1 7

1 1 1 1 1 1 1 7 1

Enterococcus

10

Escherichia Flavobacterium Klebsiella Kocuria Kurthia Lactobacillus Micrococcus Proteus Salmonella Serratia Staphylococcus

8 1 2 1 2 1 3

1 4 6 3 1

Streptococcus Streptomyces N, number of isolates.

4 1 2 1 1

40

Chapter 1

Table 1.12. Fungal intestinal ora of African dwarf crocodiles (Huchzermeyer et al., 2000). Genus Acremonium Arthrinium Aspergillus Species sp. sp. clavatus avus niger sp. guillermondii krusei sp. lipolytica luteolus sp. sp. candidum sp. sp. sp. sp. beigelii capitatum N (1993) 1 1 5 2 2 3 2 1 3 3 1 1 N (1995)

Beauveria Candida Chrysosporium Cryptococcus Curvularia Fusarium Geotrichum Paecilomyces Penicillium Phoma Trichoderma Trichosporon N, number of isolates.

1 4 2 7 2 2 1 2 1

Respiratory rate Respiration takes place in cycles of two to three rapid movements followed by a longer pause (Gans and Clark, 1976). The respiratory rate depends on the size of the animal, decreasing with increasing body mass (Gans and Clark, 1976). It is also inuenced by temperature, increasing with increasing body temperature (Campos, 1964; Smith, 1976), with lower rates during warming than during cooling (Smith, 1976). There appeared to be a low correlation between the metabolic rate and the respiratory rate (Huggins et al., 1971). Respiratory rates for different sized crocodiles are given in Table 1.13. The respiratory rate of 123 crocodiles of 27.4 min 1 reported by Sigler (1991) falls entirely outside the range of all the other observations and may possibly include pharyngeal (gular) movements. Diving The following is based on work with IndoPacic crocodiles by Wright (1987). Most voluntary dives are short, only lasting 5 min. During these dives the metabolism stays aero-

bic. Forced dives occur when the crocodile is disturbed and can last for up to 1 h. During these dives the metabolism slows down and becomes anaerobic as an oxygen debt develops. A crocodile disturbed during a voluntary dive immediately changes its metabolism. The diversion of the arterial blood ow away from muscles during forced diving conserves oxygen reserves for the functioning of the brain. Lactic acid accumulated in the muscles enters the circulation only after the crocodile emerges (Andersen, 1961). Oxygen consumption In both American alligators and Nile crocodiles, the oxygen consumption of inactive animals was found to increase as the temperature rose. However, in Nile crocodiles it was found to decrease between 25 and 30C and then rise again steeply to 35C (Brown and Loveridge, 1981; Lewis and Gatten, 1985). The decrease is seen as an adaptation to nocturnal activity, which is usually at lower temperatures (Brown and Loveridge, 1981). In the American alligator values ranging from 0.08 to 0.2 ml g 1 h 1 correspond

Crocodiles and Alligators

41

Table 1.13. Respiratory rates of crocodiles. Species Caiman crocodilus Mass (kg) 0.18 0.29 0.65 4.8 4.8 5.0 1.158.78 0.461.31 Breaths per min 0.58 0.63 0.57 0.25 0.14 0.17 3.3a:1.5b 0.394.95 Temperature (C) 2325 Reference 1 1 1 1 1 1 2 3

Alligator mississippiensis
a During b During

2325

cooling. warming. 1, Gans and Clark (1976); 2, Smith (1976); 3, Huggins et al. (1971).

with those cited from a number of reports (Lewis and Gatten, 1985). Similar values were established for the Nile crocodile (Brown and Loveridge, 1981). Non-respiratory CO2 excretion A relatively low respiratory quotient in crocodilians is explained by the excretion of large amounts of ammonium bicarbonate in the urine (Coulson and Hernandez, 1964; Grigg, 1978), while Davies (1978) suggested cutaneous CO2 loss as an explanation (see also below). Acidbase balance In American alligators and in Indo-Pacic crocodiles, arterial pH decreased with rising body temperature, while arterial PCO2 increased (Davies, 1978; Davies et al., 1982; Seymour et al., 1985; Douse and Mitchell, 1991). Respiratory regulation In progressively anaesthetized American alligators it was shown that central chemoreceptors play a signicant role in ventilatory regulation (Branco and Wood, 1993).

and uric acid in their urine, but when they are fed maximally the excretion of ammonia increases while the proportion of uric acid in the urine decreases. This decrease in uric acid clearance leads to increased plasma uric acid levels, predisposing the animals to gout (see p. 230). Only negligible amounts of urea are produced (Khalil and Hagagg, 1958; Herbert, 1981). The white deposits in crocodile urine consist mainly of uric acid crystals (Khalil and Hagagg, 1958). The glomerular ltration rate remains fairly constant under different conditions, and the tubules have little capacity to regulate the osmolality of the urine. However, cloacal absorption varies with the salt load (Schmidt-Nielsen and Skadhauge, 1967). Salt lost into the freshwater environment is replaced constantly by the salt contained in the prey. Excess salt is excreted by specialized salt glands, as is the case in other marine reptiles (Schmidt-Nielsen and Fange, 1958) (see also p. 14). Ammonia is thought to be excreted in the form of NH4HCO3 which may be responsible for a substantial decit in respiratory CO2 (Schmidt-Nielsen and Skadhauge, 1967; Grigg, 1978) (see above).

Responses to high salinity Excretion Fasting crocodiles and alligators produce approximately equal quantities of ammonia All alligatorines and most crocodiles are freshwater species with poor salt tolerance. However, four crocodile species (C. porosus, C. johnsoni, C. niloticus and C. acutus) have

42

Chapter 1

estuarine populations. Large specimens of C. acutus lose weight more slowly in sea water than small ones, and NaCl loading causes a reduction in cloacal ow rate, thus conserving body water (Ellis, 1981). Alligators osmoregulate by keeping a low body sodium turnover, by the low permeability of the skin to sodium and even by keeping a relatively low water turnover. Estuarine crocodiles add to that effect by the excreting of excess salt through the lingual salt glands (p. 14). Freshwater species of crocodiles also have these salt glands and may use them in aestivation during drought periods (Mazzotti and Dunson, 1989). Water loss through the skin when it is exposed to dry air may be considerable and the lost water can only be replaced by drinking, not absorbed through the skin (Cloudesley-Thompson, 1968).

have been described by Lance (1987). A sexsteroid-binding protein, seasonally present in the plasma of female American alligators and probably other crocodiles as well, prevents the delivery of free steroid to target organs outside the breeding season (Ho et al., 1987). Ovulation All follicles are normally ovulated together over a period of a few hours (personal communication, V.A. Lance, San Diego, 2000), but according to Youngprapakorn (1990b) sometimes some follicles ovulate prematurely and proceed through the oviduct to the uterus in advance of the others. Fertilization takes place in the infundibulum or upper oviduct before the albumen and shell are secreted in the glandular part of the oviduct (uterus). The eggs are then stored in the muscular part (vagina) until they are laid. In the American alligator the eggs are stored in the vagina for 33.5 weeks before they are laid (Lance, 1989). During this time, before oviposition, initial embryonic development is already taking place, to the 1517 somite stage and occasionally further (personal communication, V.A. Lance, San Diego, 2000). Oestradiol liberated during ovulation increases plasma calcium levels for the production of the eggshells, but, unlike birds, crocodiles do not deposit calcium in their bones before ovulation (Elsey and Wink, 1986). Nesting and incubation Nesting habits vary from species to species. Forest-dwelling species build nest mounds from leaves scooped up from the forest oor and depend on the heat produced by composting, rather than on the sun, to incubate the eggs. Swamp dwellers make nest mounts from swamp vegetation and rely on composting heat as well as on the sun for the incubation of the eggs, while crocodiles living in rivers nest in the sandy banks above the ood level and rely on the sun for incubation heat. All eggs in the clutch are deposited into the nest at the same time and covered again with nesting material. The

Reproduction Laying cycle Crocodiles reproduce by laying eggs, as the temperature control of sex determination does not allow internal incubation (ovovivipary) as occurs in some snakes and lizards. Most species lay only one clutch of eggs per year, the mugger being the exception, with two cycles per year occurring regularly (Whitaker and Whitaker, 1984). However, many females in the wild do not reproduce every year, probably depending on their nutritional state (Lance, 1987; Kofron, 1990). Clutch and egg size Egg size and egg number per clutch are species dependent but increase with the size and age of the female, with younger females laying small eggs from which fewer, smaller and more slowly growing hatchlings are produced. Hormonal control The hormonal control of the reproductive cycle and factors inuencing this control

Crocodiles and Alligators

43

incubation period depends on the species as well as on incubation temperature, decreasing with rising temperature, and ranges roughly from 60 to 90 days. Cross-breeding Several species of crocodiles cross-breed voluntarily, producing fertile hybrids (Youngprapakorn, 1990a; Thang, 1994). As these hybrids tend to be more vigorous, they are sought after by some farmers. Escaped hybrids, however, can pollute existing wild populations and this constitutes a considerable danger to the conservation of certain crocodile populations.

6.3 ml and a circulation time of 27 min (Coulson et al., 1989). Bradycardia Diving bradycardia occurs when crocodiles dive after a sudden fright. Under these circumstances the heart rate decreases from around 30 beats per minute to 25 beats per minute, but not during voluntary (shortterm) dives (Gaunt and Gans, 1969; Smith et al., 1974). During bradycardia the blood pressure is maintained by peripheral vasoconstriction (Jones and Shelton, 1993). Shunt

Circulation Blood ow The ow of blood transports oxygen and nutrients to the organs and tissues, and CO2 and end-products of metabolism from the organs and tissues to the lungs and kidneys. In addition, it can speed up the transport of heat from the skin to the internal organs when the crocodile is basking, move white blood cells and antibodies to infection sites, and hormones to targeted organs. A 70 kg American alligator at 28C has a blood ow of 0.2 l min 1, a stroke volume of 6.3 ml, a circulation time of 27 min and 4% of the metabolic rate of a person of equal mass (Coulson et al., 1989). Heart rate The heart rate depends on the size of the animal and on the temperature. In 57- to 78-cmlong American alligators at an ambient temperature of 2225C it was 18.7 beats per minute (Huggins et al., 1971). In anaesthetized American alligators from 1.5 to 4.3 kg live mass it ranged from 10 beats per minute at 10C to 30 beats per minute at 30C (Campos, 1964). At 38C and above irreversible damage occurred through overheating (Wilber, 1960). At 28C a 70 kg American alligator had a blood ow of 0.2 l min 1, a stroke volume of

Under certain conditions, venous (deoxygenated) blood can become mixed with arterial (oxygenated) blood through the foramen of Panizza, through direct release into the right aorta and through the anastomoses between the right and left aortas (see p. 23). This mixing of venous and arterial blood is referred to as a left-to-right shunt. Jones and Shelton (1993) described a biphasic systolic pressure curve in the right ventricle of resting crocodiles in which the rst phase supplies the pulmonary artery and the second phase supplies the right aorta. This shunt diverted 1525% of the venous blood away from the pulmonary circulation. They speculated that in addition to the respiratory requirements for a shunt during forced diving, the alkaline wave caused by the production of HCl in the stomach after a meal also necessitated a ow of venous (acidic) blood to the digestive viscera. Vasoconstriction Vasoconstriction is mediated hormonally and by nervous stimuli and can occur locally, e.g. as a response in thermoregulation (see below), or systemically. Adrenaline was found to produce a stronger vasoconstriction in the American alligator than noradrenaline (Akers and Peiss, 1963). Angiotensin I of the American alligator was found to be closely related to that of the chicken (Takei et al., 1993).

44

Chapter 1

Nervous activity The brain of the crocodile is larger and better organized than that of other reptiles, but it is still relatively small in relation to the crocodiles body mass. Many functions are therefore delegated to centres in the spinal cord. During hypothermia (24C) in restrained American alligators (size not stated, but probably large as their sex was stated), the electrical activity of cerebrum and optic lobes decreased, whereas it increased in the cerebellum (Parsons and Huggins, 1965). Compared with that of other reptiles, as well as with that of many birds and mammals, the hearing of crocodiles is very acute, particularly in the middle range but less so for high and low tones (Wever, 1971). On the farm, the crocodiles rely mainly on smell and hearing to recognize the person usually working with them. In nature they recognize each other by the excretions of their skin glands (see p. 52). Therefore, captive or farmed crocodiles may fail to recognize, and thus be disturbed by, people who occasionally wear perfume.

Thermoregulation Crocodiles are exothermic reptiles, unable to maintain a constant internal body temperature independently of the environment. However, they try to achieve and then maintain their temperature within a preferred range, and they do this by making use of thermogradients in the environment. These gradients exist between sun and shade, warm surface water and cool deep water. Some species also make use of burrows in which their rate of cooling during winter nights would be slower than in cold water (Pooley, 1962) or which protect them from heat and dehydration during aestivation (Christian et al., 1996). During cooling the blood circulation to the body surface is restricted, thus reducing the rate of cooling. During warming the blood ow to the skin is increased and the warmed blood transports the heat to the internal organs (Johnson, 1974; Grigg and Alchin, 1976; Johnson et al., 1976; Drane et al.,

1977; Johnson and Voigt, 1978; Smith and Adams, 1978; Smith et al., 1978; Smith, 1979). When basking in shallow water, the blood supply to the submersed skin is reduced, while it is increased to the skin exposed to the air and sun (Johnson, 1974). The osteoderms may also play a role in thermoregulation as heat collectors (Seidel, 1979). Gaping increases evaporation and thereby contributes to cooling, which at certain times of the day appears to be preferred to going into the water. However, gaping may also be used to increase the temperature-exchange surface. Consequently Nile crocodiles have been observed gaping while basking on a cold African winter morning (own observation). The preferred temperature depends on the crocodiles activity: fasting crocodiles prefer cooler and feeding ones select higher temperatures (Lang, 1979). Endogenous (metabolic) heat plays a role only in very large crocodiles with a low surface area to mass ratio (Smith, 1979). In very cold winter weather American alligators remain close to the surface, with only the nostrils protruding from the water. In this position, called icing, they are safe from suffocation when the water freezes over (Hagan et al., 1983; Lee et al., 1997). However, even such specimens do not survive if their internal temperature falls below 4.5C (Brisbin et al., 1982). A released American alligator in a swamp in Pennsylvania appears to have survived at least six cold winters before it was shot (Barton, 1955). Nile crocodiles tolerate a minimum internal temperature of 10C. Exposing juvenile farmed crocodiles to varying temperature regimes, Turton et al. (1994) found that high temperatures are more stressful than lower ones, and that temperature changes are always accompanied by increased corticosterone levels. Certain farming conditions tend to expose the crocodiles periodically to overheating as well as to widely uctuating daynight temperatures, a situation that is obviously to be avoided. It is my belief that for their well-being crocodiles need to be able to thermoregulate actively along a thermogradient within the range of preferred temperatures. They

Crocodiles and Alligators

45

should also be strictly protected from forced overheating, i.e. being exposed to high temperatures without any means of avoiding the heat or being able to cool down. The growth rate of juvenile crocodiles is closely related to the temperature at which they are kept, with the fastest growth seen in those kept closest to the preferred maximum temperature, and particularly in those with the highest preferred temperature (Lang, 1987). As the preferred temperature is inuenced by the incubation temperature, one can actively select for a higher temperature preference, and thus for faster growth, by incubating at a higher temperature (Lang, 1987).

Immunity Crocodiles can react to infections by developing antibodies and thus becoming immune to the agent in question. The white blood cells that play a role in this system

have been described above (p. 25). In response to a stimulus, lymphocytes are produced in the thymus and spleen. An active spleen increases in size very rapidly, but as the tough brous capsule resists this rapid growth, the active tissue buds out through the capsule, giving the hypertrophic spleen an irregular, knobby appearance (Fig. 1.46). Unlike other reptiles, crocodiles are capable of an anamnestic response. Young American alligators immunized with 50 mg haemocyanin had antibodies in their blood after 20 days. However, when given a second injection of 2.5 mg, antibodies became detectable after only 2 days (Lerch at al., 1967). An immunoglobulin with two IgG-like light chains was isolated from American alligators by Saluk et al. (1970). Turton et al. (1994) isolated an immunoglobulin from juvenile Indo-Pacic crocodiles and identied it as IgG, with a molecular weight of 218 kDa and heavy and light chains of 57 and 27 kDa, respectively.

Fig. 1.46. Budding hypertrophic spleens as a consequence of an immune response.

46

Chapter 1

American alligators did not have any isohaemagglutination, but their serum contained three agglutinins, one for all human cells, another similar to the -agglutinin and one similar to the -agglutinin of human serum (Bond, 1940). Inammation Exudation Inammation is a reaction by the body to localize, isolate and ght a local infection or other injury. The rst step is a congestion of the local capillaries, allowing serum to seep into the tissue and cause oedema. In mammals, the liquid from this oedema is ltered with the lymph through lymph nodes, but crocodiles, like birds, lack lymph nodes. To prevent the drainage of pathogens away from the inammation site directly into the general circulation, they exude brin into the inamed site, which immobilizes all the pathogens and prevents their escape. This is a very successful strategy, with the result that crocodiles and birds rarely contract septicaemia from wound infections. However, if the inammatory cells are unable to remove the invading pathogens, the exudation process continues and ultimately can lead to serious problems. Abscess, briscess Fibrin also inhibits the movement of leucocytes and prevents the liquefaction of necrotic tissue, with the result that true abscesses lled with liquid pus cannot be formed. Hard swellings forming at the site of an infected wound consist of sheets of brin between the tissues and these are extremely difcult to remove surgically. Veterinarians often refer to this exudate erroneously as inspissated pus. Since such a brin-lled swelling cannot be classied as a true abscess, it should rather be called briscess (Huchzermeyer and Cooper, 2000). Cellular reactions After subcutaneous injection of turpentine into juvenile American alligators, Mateo et al. (1984b) observed oedema followed by gran-

ulocyte migration in the rst 3 days. Later monocytic cells predominated, including vacuolated macrophages. From 14 days onwards zones of necrotic debris (most likely exudate, see above) were surrounded by palisades of vacuolated multinucleated giant cells and capillary-laden immature brous connective tissue.

Fever Fever results from a higher setting in an animals thermoregulatory system in reaction to an infection or similar event. In endotherms the increase in temperature is achieved metabolically, but crocodiles, as ectotherms, have to adjust their temperature behaviourally by selecting a higher temperature on the environmental gradient (Lang, 1987) (see p. 44).

Disease In a holistic view, a healthy animal lives in a state of balance with its natural environment. Within certain ranges it can respond to all physical, chemical and biological challenges. These challenges may act singly or in combination (Fig. 1.47). The responses are the defences. An animal that is unable to defend itself adequately against any such single or combined challenge slides into a state of imbalance that is referred to as disease (Wedemeyer et al., 1976). Captive, farming and ranching conditions are usually different from natural conditions and often far from ideal. Often they increase the severity of the challenges while limiting the animals ability to respond. Such conditions can easily cause an animal to become imbalanced and diseased. From the holistic denition of disease it is clear that such a state cannot be diagnosed merely by examining the affected animal alone, nor by the laboratory analysis of certain specimens taken from the diseased or deceased animal. In addition, all factors in the environment, as well as nutrition, have to be taken into consideration. Equally, all contributing environmental and other factors must also be considered when formulating a

Crocodiles and Alligators

47

Fig. 1.47. Schematic drawing of the physical, chemical and biological challenges countered by the appropriate responses of the crocodile in a state of balance.

course of treatment or a prophylactic programme. It is for this reason that chapters on behaviour, nutrition and farming practices have been included in this book. It is of little use if in a diagnosis the terms stress and poor management are used without clarifying the exact circumstances involved in the particular case, nor does the isolation of a pathogen from a crocodile necessarily mean that this was the primary cause of disease or death. Also, none of the crocodile-specic pathogens (viruses, bacteria, etc.) are primary pathogens. All are opportunists, waiting for a weakened or stressed animal in which to produce the specic disease. In all such cases one should always ask: Why did this happen? One should always investigate the circumstances of the outbreak. In a way, it is unfortunate that in a book like this the individual diseases have to be discussed in relation to their causal agent, when in reality they are all inuenced or even triggered by environmental factors.

Blood biochemistry Published values of the blood (serum, plasma) biochemistry of crocodilians are given in Tables 1.14 to 1.16. Since most of these values are from captive or farmed animals, there may be some doubt as to whether they can be taken as normal values. Species differences may play a role and the stress involved in immobilizing the animals for sampling might also affect the results. However, they may still give some guidance for the interpretation of results of clinical investigations. In addition, thyroxine values are given in Table 1.17. In juvenile American alligators the injection of alligator, turkey or bovine insulin caused a hypoglycaemia lasting from 12 to 120 h after the injection, and a much more rapid decrease in plasma amino acids lasting from 2 to 36 h after the injection (Lance et al., 1993). All blood chloride, bicarbonate, pH and sodium values should be determined on animals that have been fasting for at least 3 days. This is because far-ranging changes are brought about by the alkaline tide following the ingestion of food, with all the accompanying changes in blood electrolytes (Coulson et al., 1950).

Crocodilian Biochemistry
This section concentrates on diagnostic biochemistry, trying to give normal values, as far as they are known.

48

Chapter 1

Table 1.14. Blood biochemistry of farmed and captive crocodiles. Parameter Total protein Albumin Globulin Glucose Calcium Phosphorus Sodium Potassium Magnesium Chloride Total serum iron Uric acid Urea Bilirubin Cholesterol Triglyceride Creatinine GOT GPT ALP ALT AST BUN T4 T3 rT3 LDH Unit g dl 1 g dl 1 g dl 1 mg dl 1 mmol l 1 mg dl 1 mmol dl 1 mg dl 1 mmol dl 1 mmol dl 1 mmol dl 1 mmol dl 1 mmol dl 1 mol dl 1 mg dl 1 mol dl 1 mg dl 1 mg dl 1 mg dl 1 mmol l 1 mmol l 1 mg dl 1 mg dl 1 mol dl 1 IU l 1 IU l 1 IU l 1 IU l 1 IU l 1 mg dl 1 nmol l 1 nmol l 1 nmol l 1 IU l 1 A.m.a 5.21 1.87 3.33 92.0 10.73 5.73 144.2 3.71 104.2 3.03 8.17 3.8 0.16 120.8 231.5 0.47 110.5 1.17.2 0.18.8 1.06 16.6 13.1 30.03 46.05 223.5 0.99 4.95 0.2 0.7 46.2 0.21 2051 18.0 20.2 17.8 4.1 C.l.b C.m.c 9.37 C.n.d 5.3 1.9 3.1 81.6 2.42.8f T.s.e 3.7 C.p.g 4.17.0 1.42.3 2.75 4.512.1 10.5 3.0 10.2 2.413.45 3.4 155.9 4.4 120.0 3.2 167988 1.22.9 143161 3.87.2 0.81.4 88127 119

81.82

52.95

75.3

31180 1151 23157

1.45

426.2

A.m., Alligator mississippiensis; C.l., Caiman latirostris; C.m., Crocodylus moreletii; C.n., Crocodylus niloticus; T.s., Tomistoma schlegelii; C.p., Crocodylus porosus. a Barnett et al. (1998); b Tourn et al. (1994); c Sigler (1991); d Foggin (1987); e Siruntawineti and Ratanakorn (1994); f Morpurgo et al. (1992); g Millan et al. (1997a). GOT, glutamate oxaloacetate transaminase; GPT, alkaline phosphatase; ALP, alkaline phosphatase; ALT, alanine aminotransferase; AST, alanine transaminase; BUN, blood urea nitrogen; T4, thyroxine; T3, triiodothyronine; rT3, reverse triiodothyroxine; LDH, lactate dehydrogenase.

Urine biochemistry The nitrogenous wastes excreted by the kidneys consist of uric acid, urea and ammonia in the form of ammonium bicarbonate (NH4HCO3). Crocodile urine, like that of birds, consists of a liquid and a solid portion. Values determined from the liquid urine of fasting crocodiles are given in Table 1.18. The

urine solids of the Nile crocodile were composed of 6% ammonia and 88.6% uric acid; no urea was present (Khalil and Haggag, 1958). The full composition of the urine of fasting American alligators is given in Table 1.19. In a comparison between maximally fed American alligators (fed ad libitum ve times per week) and those given a single large meal, it was found that uric acid excretion levels were sim-

Crocodiles and Alligators

49

Table 1.15. Clinical serum biochemistry: means of 2-year-old farmed Nile crocodiles (n = 5) (Thurman, 1990) and ranges of means of wild Nile crocodiles from three different rivers in the Kruger National Park, South Africa (Swanepoel et al., 2000). Parameter Albumin Globulin Glucose Na K Ca Mg SIP TSP LD ALP CK Lactate Cortisol Urea Creatinine Cl Unit gl 1 gl 1 mmol l mmol l mmol l mmol l mmol l mmol l gl 1 IU l 1 IU l 1 IU l 1 mol l nmol l mmol l mmol l mmol l Farmed Wild 9.816.38 30.747.35 3.211.45 141.5154.5 2.535.35 2.603.98 1.512.24 0.881.96

Table 1.17. Mean plasma thyroxine values of crocodiles. Thyroxine (ng ml 1) Crocodylus niloticus (Morpurgo et al., 1992) Crocodylus johnsoni (Hulbert and Williams, 1988) 1.63 2.5

1 1 1 1 1 1

5.9 153.8 3.8 2.97 0.52 50.2 301 64.2 211 22.1 <27

Table 1.18. Percentage distribution of nitrogen in the liquid urine of fasting crocodiles. Crocodylus niloticus (Khalil and Haggag, 1958) 66.8 12.5 2.3 Alligator mississippiensis (Hopping, 1923) 6681 017 719.8

Component Ammonia Urea Uric acid 0.602.62 36.597.0 88.5120.5

1 1 1 1 1

Mineral values Plasma Plasma mineral values of wild and farmed male American alligators, lengths ranging from 185 to 325 cm (wild) and 230326 cm (farmed) (Lance et al., 1983), are shown in Table 1.20. Organs For organ mineral values of American alligators and Nile crocodiles see Tables 6.1 and 6.2.

SIP, serum inorganic phosphate; TSP, total serum protein; LD, lactatedehydrogenase; ALP, alkaline phosphatase; CK, creatine kinase. Table 1.16. Blood biochemistry of Caiman latirostris (means only). Parameter Calcium Creatinine Phosphate Glucose Urea Cholesterol GOT GPT LDH Total protein Albumin Globulin Unit mg dl mg dl mg dl mg dl mg dl g dl 1 IU l 1 IU l 1 IU l 1 g dl 1 g dl 1 g dl 1
1 1 1 1 1

Troiano and Tourn et al. Althaus (1993) (1993) 10.12 0.36 5.40 102.2 6.88 2.315 163 19.67 1020 5.01 2.42 3.10

Bones The mean mineral composition of the ribs of three wild Nile crocodiles from the Kruger National Park, South Africa, was: Ca, 17.9%; P, 7.9%; Mg, 0.38%; F, 713 g g 1 (Swanepoel et al., 2000). It is quite possible that the skull and legs of crocodiles have a higher density than the ribs.

GOT, glutamate oxaloacetate transaminase; GPT, alkaline phosphatase; LDH, lactate dehydrogenase.

ilar in both groups, while the excretion of ammonia was low in the single-meal group. However, uric acid clearance was also low in the single-meal group, with high levels of plasma uric acid (Herbert, 1981) (see p. 41).

Composition of crocodile fat The fatty acid composition of the plasma and of the body fat depend on the sources of fat in the food, but also varies according to the

50

Chapter 1

Table 1.19. Urine composition of fasting American alligators expressed per kg body mass per day (Coulson and Hernandez, 1964), unit abbreviations as used by the authors. Parameter Volume pH OP NH2 K Na Ca + Mg CO2 as bicarbonate Cl P SO4 Uric acid N Creatinine OP, osmotic pressure. Table 1.20. Plasma minerals of wild (n = 24) and farmed (n = 1823) male American alligators (Lance et al., 1983). Parameter Calcium Magnesium Zinc Copper Iron Selenium Protein Cholesterol Vitamin E Unit mmol l 1 mmol l 1 g ml 1 g ml 1 g ml 1 g ml 1 gl 1 mg l 1 g ml 1 Wild 3.12 1.32 0.44 0.76 0.53 0.17 0.564 5.81 5.36 Farmed 2.87 1.06 0.42 0.60 0.54 0.2 0.553 5.02 5.25 Table 1.21. Lipid composition (%) of American alligator fat from two farms (Peplow et al., 1990). Triglyceride Diglyceride Monoglyceride Free fatty acids Cholesterol Phospholipid 77.2 2.4 0.4 1.9 1.8 4.8 85.1 2.1 1.5 1.2 0.2 6.7 Unit ml mOs l 1 mEq l 1 mEq l 1 mEq l 1 mEq l 1 mEq l 1 mEq l 1 mEq l 1 mEq l 1 mM l 1 (?) mg l 1 Mean 17 7.81 203 1.77 0.13 0.06 0.03 1.19 0.05 0.45 0.17 0.75 0.6 Range 628 7.67.93 157247 0.672.4 0.010.26 0.010.1 0.020.05 0.461.47 Traces to 0.12 0.070.98 0.10.26 0.182.14 0.371.04

Table 1.22. Fatty acid composition (%) of American alligator fat from different trial groups and different farms (Peplow et al., 1990). Fatty acid Low 1.3 0.00 19.9 4.4 3.1 33.2 3.4 0.9 1.1 0.01 0.1 0.00 0.7 0.00 High 3.3 0.19 22.1 7.7 8.4 44.4 19.3 3.4 2.8 0.17 4.0 0.98 11.1 0.14

species of crocodile (Tables 1.211.26). The different crocodilian species may, in fact, have differing nutritional requirements for saturated and unsaturated fatty acids. A homeostatic mechanism may be lacking, but there may also be an age effect (Morpurgo et al., 1993a; Gelman and Morpurgo, 1994; Morpurgo and Gelman, 1995).

Nutrient composition of crocodile eggs Yolk The lipid and fatty acid composition of American alligator eggs and the changes during incubation were described by Noble et al. (1993). The composition on day 8 of incubation is shown in Tables 1.27 and 1.28.

C14:0 C14:1 C16:0 C16:1 C18:0 C18:1 C18:2 C18:3 C20:1 C20:2 C20:5 C22:1 C22:6 C24:1

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51

Table 1.23. Fatty acid composition (%) in four groups of juvenile Indo-Pacic crocodiles (Garnett, 1985). Fatty acid C16:0 C18:0 C16:1 C18:1 C18:2 C18:3 C20:4 C20:5 C22:6 Newly hatched 19.62 5.93 2.95 30.31 5.01 1.70 3.22 7.75 15.55 Starved 22.81 9.99 2.26 35.27 8.43 1.62 7.31 0.60 2.84 Fed lean pork 21.86 8.59 2.84 29.22 21.18 2.81 3.37 1.07 2.52 Fed fatty pork 22.73 12.19 2.94 41.06 11.31 1.85 1.26 0.17 0.41

Table 1.24. Mean percentage plasma fatty acid composition in 3- and 8-year-old farmed and 36-yearold wild Nile crocodiles (Morpurgo et al., 1993a). Fatty acid 16:0 16:1 18:0 18:1 18:2 18:3+20:1 20:4 20:5 22:5 22:6 Farmed (3 years old) 38.46 0.60 9.22 19.11 20.32 2.79 6.82 1.25 0.22 1.50 Farmed (8 years old) 37.04 4.95 9.94 23.74 22.79 0.69 3.58 0.46 0.34 0.31 Wild 27.03 7.49 12.54 27.00 12.04 3.44 2.71 2.74 1.25 3.91

NB: The tables in the paper by Morpurgo and Gelman (1995), referring to the same results, appear to have been mixed up. Table 1.25. Fatty acid composition of crocodile meat (Crocodylus porosus and Crocodylus johnsoni), averages of 12 samples (Mitchell et al., 1995). C:n 14:0 15:0 16:0 16:1 16:1 17:0 18:0 18:1 18:2 18:3 18:4 20:0 20:1 20:4 20:4 20:5 22:5 22:5 22:6 Name Myristic Pentadecanoic Palmitic -9 -7 Palmitoleic Heptadecanoic Stearic Oleic Linoleic -Linolenic Arachidic Gondoic Arachidonic Eicosapentaenoic Docosapentaenoic Docosahexaenoic % 1.1 0.2 22.5 0.4 5.1 0.5 7.4 33.1 15.2 4.8 0.1 < 0.1 0.5 3.6 0.3 0.5 0.4 1.5 1.3 Table 1.26. Fat prole of boiled tail meat of Alligator mississippiensis means in % (Debyser and Zwart, 1991). Total fat content Saturated fat Mono-unsaturated fat Poly-unsaturated fat Cholesterol (mg/100 g) 2.9 29.1 46.5 24.0 64.8

-9 -6 -3 -3 -9 -6 -3 -3 -6 -3 -3

Table 1.27. Mean yolk lipid composition (% of total lipid) of American alligator eggs incubated at 30C on day 8 (Noble et al., 1993). Cholesteryl ethers Triacylglycerols Free fatty acids Free cholesterol Phospholipids 1.48 69.5 1.60 7.68 19.8

52

Chapter 1

Table 1.28. Mean fatty acid composition (% of total) of the cholesteryl esters, triacylglycerols and phospholipids of the yolks of incubated American alligator eggs on day 8 (Noble et al., 1993). Fatty acids Palmitic Palmitoleic Stearic Oleic Linoleic Linolenic Arachidonic Docosapentaenoic Docosahexaenoic Cholesteryl esters 60.0 5.68 7.76 16.4 4.47 1.69 3.96 <1.0 <1.0 Triacylglycerols 29.1 18.5 6.49 32.3 6.53 4.58 1.02 <1.0 <1.0 Phospholipids 32.1 9.16 7.88 19.3 4.18 2.33 13.1 2.38 9.67

Albumen The albumen of avian eggs consists largely of proteins with antibacterial properties. Crocodile egg albumen contains much fewer solids (3.6% against 12% in birds) and the main protein is a glycoprotein (Burley et al., 1987; Abrams et al., 1989; Rose et al., 1990). An 2-macroglobulin-like protease inhibitor was identied in the albumen of eggs of the Cuban crocodile (Ikai et al., 1983). The possibility that the proteins in crocodilian eggs have antibacterial properties has not yet been investigated.

Paracloacal and gular glands The secreta of the paracloacal and gular glands are used by all crocodilians for chemical signalling. This is important for the recognition of individuals, of the sex of any other individual and of conspecics. The paracloacal glands of C. crocodilus and Caiman latirostris contained between 3.5 g and 34.5 g secreta. They consisted of fatty acids, particularly myristic and palmitic acid, nitrogenous bases, glycerol, cholesterol, traces of phosphorus-containing compounds and an eight-carbon alcohol, yacarol. This was later identied as D-citronellol and was characterized by its distinct rose-like scent (Fester and Bertuzzi, 1934; Fester et al., 1937). Citronellol was also found in the paracloacal gland secreta of Paleosuchus palpebrosus and P. trigonatus (Shafagati et al., 1989). The diterpene -springene that occurs in the paracloacal glands of P. trigonatus is also present in the secretions of a braconid wasp and of the

springbok antelope, as well as in tobacco leaves (Avery et al., 1993). Paracloacal secreta of 80 immature and 15 adult American alligators contained hexadecyl and other acetates and esters, but no free alcohols. There was a high degree of variation between age classes and sexes, but also individually (Weldon et al., 1988). The secreta of the gular glands of American alligators consist of C14, C16 and C18 fatty acids, squalene and -tocopherol, but contain no pheromone (Weldon et al., 1987). Lipids from the paracloacal glands of adult Chinese alligators of both sexes consisted of acetates, aliphatic alcohols, free fatty acids and waxes, primarily hexadecanoates. The male secretions also contained cholesterol, a diterpene hydrocarbon, cembrene A and a diterpene ketone (Dunn et al., 1993; Mattern et al., 1997). The secretions of the paracloacal glands of O. tetraspis contained an aromatic ketone, dianeackerone, and several aromatic steroidal esters (Whyte et al., 1999; Yang et al., 1999). A comparative chromatographic study of the secretions of gular and paracloacal glands of almost all crocodilian species, except C. novoguineae, was carried out by Weldon and Tanner (1991).

Crocodilian Behaviour
Normal behaviour is characteristic of a healthy animal. Not to be able to act in accordance with its behavioural requirements in a captive or farm situation may severely stress an animal. Non-domesticated animals, par-

Crocodiles and Alligators

53

ticularly crocodiles, are very sensitive to this kind of stress. It is therefore important for crocodile farmers and veterinarians to be aware of the behaviour patterns and requirements of their crocodiles.

Embryonic learning It has been found that the food selection of Indo-Pacic crocodiles can be inuenced by painting avours on to the crocodile eggs during incubation (Sneddon et al., 1998). This kind of embryonic learning may also inuence other aspects of hatchling behaviour. It is possible that by urinating on the nest the mother primes the hatchlings to recognize her when they hatch.

farmed Nile crocodiles in South Africa was reported by Huchzermeyer (1998b). It is postulated that when the mother drives the hatchlings away before the new brood hatches (see below), a behavioural switch is operated, inducing the juveniles to avoid larger crocodiles from then on. When farmreared juvenile crocodiles are released into the wild, often many of them are eaten by older crocodiles. Possibly their lack of imprinting made them unable to see the danger posed by larger members of the same species.

Dispersal of the young Before the new clutch hatches, in some species possibly long before, the juveniles leave their mother, and there are some indications that, in fact, they are being actively chased away (Hunt, 1977; Hunt and Watanabe, 1982). After leaving their parents they may still stay together in pods, even pods consisting of several clutches (Allstead, 1994), or they may disperse individually. In many species the different age groups occupy different habitats, primarily for agespecic prey requirements, but also keeping the different sizes apart and thereby minimizing cannibalism.

Parental care Parental care has been observed in many crocodile species and it is presumably the rule in all crocodilians. It includes guarding the nest, helping the hatchlings out of the egg, carrying them from the nest to the water, guarding them there, responding to the distress calls of young ones in danger and occasionally moving the pod to new nursery areas. All this is done mainly by the female, but, where the adults live in pairs or where the female has disappeared, males have been seen either helping or taking over the care of the hatchlings (Alvarez del Toro, 1968).

Cannibalism Cannibalism occurs quite commonly in crocodiles and may be regarded as a population regulatory mechanism, allowing more juveniles to reach adulthood in a depleted adult population (Hutton, 1989). However, high losses of released juveniles (Rootes and Chabreck, 1993) could also be caused by the fact that the released farm-reared animals were non-imprinted and therefore did not have the behavioural switch enabling them to avoid larger members of the same species (see above). Where the size classes are segregated in the wild, it would be important to release juveniles into the correct habitat or niches to avoid excessive cannibalism. The fact that many sporulated coccidian sporocysts often become sequestered in dif-

Imprinting Imprinting is known from birds, which at hatch are imprinted with the image of their mother and thereby recognize their parents and later in life choose their sexual mate in their parents image. Human imprinting in intensively reared ostrich chicks can lead to behavioural disturbances, sometimes with serious consequences (Huchzermeyer, 1996a). It is difcult to explain the complex hatchlingparent interactions of crocodilians without thinking of the possibility of imprinting. A suspected case of human imprinting of

54

Chapter 1

ferent organs of crocodiles (see p. 187) could also be an indication that cannibalism is a normal occurrence in crocodiles in the wild and that this parasite, at least, has adopted this as a mechanism for its transmission.

Hunting and feed selection Crocodiles are nocturnal animals and hunt or forage actively during the night. However, they will also take prey during the day if the opportunity should arise. How much their behaviour is affected by diurnal feeding in captive and farm situations is not known. However, crocodiles might become more interesting for zoo visitors to observe if they were shown in a night display. All crocodiles prefer live, moving food, but they easily adapt to inert feed, such as fresh or boiled mince. Under suitable stressfree conditions they also will take pelleted feed without any problems. While small sh, tadpoles, frogs and toads were readily recognized as prey by Nile crocodile hatchlings previously fed with mince, lizards (Agama stellio) were left untouched (Morpurgo et al., 1991).

diles during the breeding season. In general, one can say that swamp-inhabiting crocodiles are stricter about establishing territories, while riverine species tend to be more gregarious or tolerant of a higher population density in a breeding area. This may have implications for the establishing of breeding colonies on crocodile farms. Although apparently severe wounds may be inicted during territorial ghts between males, the ghts are more of a ritualized nature (Plate 4) and much less severe than those between females over nesting sites.

Sexual behaviour The sexual behaviour of crocodiles consists of courtship displays, mating and defending the harem. Here also the details differ from species to species. Often, while the dominant male is occupied with one particular female, some of the other females of his harem will seek out and copulate with other males. This leads to multiple fatherhood of particular clutches and has the benet of a wider spread of genes. In large breeding colonies on Nile crocodile farms one aims to provide distinct territories for several dominant males by the disposition of islands and other visual barriers (Fig. 1.48).

Social behaviour Social interactions revolve around sexual, territorial and food competition, and the establishment of a ranking hierarchy in a population. For this the crocodiles use acoustic and visual signalling as well as aggression. The signals vary to some extent from species to species, and so does aggressiveness. In juvenile farmed Nile crocodiles, aggression was found to be linked to feeding and the type of feed, to stocking density and to size variation. Inert feed, low stocking density and removal of the larger individuals were all conducive to low aggression levels (Morpurgo et al., 1993b).

Nesting Depending on the characteristic habitat of the species, crocodiles either build nest mounds from the substrate (vegetation matter or sand) or dig holes in the sand. It is believed that the rotting vegetation in the nest mound contributes to the creation of the correct incubation temperature, particularly in dense forest, where the nest mounds cannot be exposed to the sun. In areas where ooding occurs, crocodiles choose high ground for their nesting sites. For this reason it is important when designing breeding colonies on Nile crocodile farms to have all the nesting sites at the same level, to avoid competition for the more elevated ones (Fig. 1.49).

Territoriality Territorial behaviour varies from species to species and is most marked in adult croco-

Crocodiles and Alligators

55

Fig. 1.48. Breeding colony on a Nile crocodile farm with visual barriers to allow the establishment of several individual territories.

Fig. 1.49. Nesting sites all on the same level in a breeding colony for farmed Nile crocodiles.

Thermoregulation All crocodiles like to maintain a constant internal body temperature, depending somewhat on their activities and the time of day. To achieve this they make use of the environmental thermogradient, which consists of sun (radiation) and shade (air temperature), as well as warm surface and cool

deep water. To some extent they can also make use of evaporative cooling, although it is unlikely that that is the only purpose of gaping (Fig. 1.50). During gaping the gular valve remains closed, whereas it opens during yawning. Many species make use of burrows to escape excessive heat (aestivation) or excessive cold. This means of maintaining the

56

Chapter 1

Fig. 1.50. Gaping Nile crocodile on a farm in South Africa; gaping may facilitate evaporative cooling.

temperature is usually not provided on crocodile farms. In autumn, Chinese alligators dig particularly elaborate burrows, with one or two openings usually facing south, one or two tunnels, one to three chambers, a sleeping platform and a pool. They use their snout, fore limbs, body and tail for digging and moving the soil (Bihui et al., 1990). We also know the pleasures of thermoregulatory behaviour, lying on a beach and soaking up the warm sunshine, then diving into the cold water to cool down, and then back into the sun again and so on. Crocodiles lying in the sun the whole morning are not just lying there, they are busy thermoregulating. We should always keep in mind that to prevent crocodiles in a captive or farm situation from being able to thermoregulate and achieve their desired temperature can cause very severe stress. Optimal core temperatures are between 28 and 33C. Temperatures above 35C are lethal (once the internal temperature rises to those levels), and several systems cease to function below 25C. However, American alligators are known to survive very low temperatures. If, during a cold spell, their water freezes over, they keep their nostrils out of the water (ice), while the rest of the body remains submerged. This behaviour is called icing (Hagan et al., 1983; Lee et al., 1997) (see also p. 44).

Vocalization Crocodiles have a large repertoire of sounds that they use in their various interactions. This begins with the croaking of the hatchlings in the egg when they are ready to hatch, their frequent croaking to inform their mother and hatch mates of their whereabouts, and the distress call of a hatchling in danger. The same distress call is also used by older juvenile crocodiles. In some species vocalizations are added to the mating displays. Growling and bellowing are used to threaten off attackers or competitors. In the Congo Basin swamp forests, adult African dwarf crocodiles can be heard calling each other during the night (own unpublished observation). Britton (2001) has classied the calls of juvenile crocodilians as: hatching calls; contact calls; threat calls; annoyance calls; distress calls.

Their vocal range includes infrasound, which may be audible to other crocodiles in the water over very long distances. The agitation of the water around the thorax of an American alligator producing this sound is shown in the cover photo of Volume 1 of the 1990 CSG Proceedings (CSG, 1990).

Chapter 2
Examination of Crocodiles and Clinical Procedures

Clinical Examination
Capture and physical restraint Stress The capture of wild crocodiles falls outside the scope of this book. The subject here is the handling of captive and farmed crocodiles. All handling and physical restraint causes severe stress and should therefore be kept to the minimum. If it is ever necessary, the least violent methods should be employed.

Bare hands Hatchlings can be caught by hand directly behind the head. Slightly larger juveniles are caught in the same way, but the tail is held with the other hand. A dustpan held over the crocodile to be caught will be accepted as shelter. The hatchling or juvenile will remain immobile under the shelter and can easily be apprehended by the free hand (Fig. 2.1). Specimens over 1 m in size are caught with a wet towel (Blake, 1993), the animal to be caught is separated from the others and a

Fig. 2.1. Holding a dustpan over the hatchling to be caught. CAB International 2003. Crocodiles: Biology, Husbandry and Diseases (F.W. Huchzermeyer) 57

58

Chapter 2

wet towel or sack is thrown over its head (Fig. 2.2). The handler then grabs the caudal part of the head through the towel, while straddling the crocodile and holding its body between his knees (Fig. 2.3). With larger animals a second and third person may be needed to hold down the body and tail. Another assistant then secures the jaws with insulating tape, taking care not to block the nostrils. The muscles opening the jaws are relatively weak, so the crocodile will be unable to break the insulating tape.

Therefore, using rubber bands or string is not necessary and can cause needless discomfort. The animal can be further immobilized by tying it to a plank, pole or ladder (Fig. 2.3). In this way it can also be carried to another location (Fig. 2.4). Bending the body sideways and fastening the head to the tail prevents the crocodile from rolling in attempts to free itself. Pressing the eyes into the orbits and then taping the eyes shut appears to have a further calming effect (Fig. 2.5).

Fig. 2.2. A wet sack is thrown over the head of the roped crocodile.

Fig. 2.3. The crocodile is tied to a ladder, while one assistant sits on its head.

Examination of Crocodiles and Clinical Procedures

59

Fig. 2.4. The crocodile tied to a ladder can now be moved without danger to the assistants.

Fig. 2.5. Young Nile crocodile with jaws and eyes taped closed. Note that masking tape is not a suitable material as it is not water resistant.

Devices The above methods are very stressful for the animal and also dangerous for the handler(s) and it is better to use one of the handling devices described below. Hatchling and small juveniles (<1 m) are easily caught with snake tongs (Fig. 2.6) or Pillstrom tongs (McDaniel and Hord,

1990). This allows one to catch them from a distance without having to enter the rearing pen and thereby upsetting all the other hatchlings in the pen. A catching noose made from strong rope can be handled more easily if it is passed through a strong PVC pipe of adequate diameter and length (Fig. 2.7) (Fletcher and Trammel, 1989).

60

Chapter 2

Fig. 2.6. Snake tongs can be used to catch crocodile hatchlings out of their pen without causing disturbance.

Fig. 2.7. Catching noose tted through a PVC pipe.

PVC irrigation pipes of various diameters and lengths can be used to restrain and transport crocodiles after they have been caught with a noose around the neck and a second noose has been tted around the body in front of the hind legs. The front noose is used to pull the crocodile into the pipe and the rear noose is then used to hold it back, preventing it from escaping through the front of the pipe (Fig. 2.8) (Jones and Hayes-Odum, 1994). Both ropes can be fastened through holes or notches drilled or cut into the pipe. A rigid PVC pipe of about 58 cm diameter is also useful for chasing away other crocodiles while working in the pen, e.g. when collecting eggs. Such a pipe produces a loud noise when hitting the

ground next to the crocodile that is to be chased away. This noise is very similar to the jaw clap used by crocodiles as a warning, and this is probably why it is so effective. Being lighter than a pole of similar dimensions, its impact is lighter and there is less danger of causing pain or injury when hitting the crocodile.

Physical examination Unrestrained crocodiles An unrestrained crocodile is examined from a distance in its enclosure. Its estimated length is noted and its nutritional state is judged mainly by the relative thickness of its

Examination of Crocodiles and Clinical Procedures

61

Fig. 2.8. Crocodile inside a large PVC pipe, held in place by two ropes which are fastened into notches in the pipe.

neck, a severely drawn-in neck being typical for an animal in a poor state (Fig. 2.9). Sunken muscles in the supertemporal fossae (see p. 7) also indicate a poor state of nutrition (Fig. 2.10). Nile crocodiles can be recognized individually by the distribution of dark spots on both sides of the tail, and the same probably holds true for some of the other crocodile species (Swanepoel, 1996) (see p. 74). The tail lying either erect or at in a sideways posi-

tion is supposed to indicate the state of health, the latter position indicating poor health (Fig. 2.11), but this is rather doubtful. The animal is then examined for obvious abnormalities, wounds, other skin lesions or discoloration and also the state of its eyes. Restrained animals Restrained crocodiles can be examined more closely. They can also be turned over for a

Fig. 2.9. A drawn-in neck indicating a poor state of nutrition.

62

Chapter 2

Fig. 2.10. Sunken supertemporal fossae on a captive Nile crocodile, indicating a poor nutritional state (photo Henri Lagasse).

Fig. 2.11. A tail lying at on its side, supposedly indicating poor health.

close examination of the belly skin and cloaca. The eyes are difcult to examine, as they are retracted as soon as the lids are touched. However, it is possible to examine the pupil and its response to light, as well as the eyelids for any sign of conjunctivitis. A whitish dis-

coloration of the eyelids and the area around the nostrils sometimes occurs in chronic disease conditions (Fig. 2.12) (see p. 237). The whiteness of the teeth of hatchlings and older crocodiles indicates the state of calcium nutrition. Calcium-decient croco-

Examination of Crocodiles and Clinical Procedures

63

Fig. 2.12. A whitish discoloration around the nose may indicate a chronic disease condition.

diles have clear, diaphanous, glassy teeth (Fig. 2.13), and such hatchlings should be tested for the rigidity of their bones by gently trying to bend the upper jaw (rubber jaw) (see pp. 148 and 211). In hatchlings the mouth can also be opened, by a gentle tap on the nose, to examine the gingivae, the tongue and the two aps of the gular valve (see p. 11).

Diagnostic imaging While wild and farmed crocodiles can rarely be taken to imaging apparatus, this situation may be different in the case of captive animals, as many zoos and specialized city practices have well-equipped clinics and laboratories. However, the existing literature on this subject is still very limited:

Fig. 2.13. Diaphanous teeth in a calcium-decient adult Nile crocodile.

64

Chapter 2

Radiography: radiographs were taken of the digital connective tissue masses of an American alligator at San Diego Zoo (Ensley et al., 1979). No technical details were given. Ultrasonography: ultrasound was used to evaluate follicle development in adult female broad-nosed caimans (Vac et al., 1992; Verdade, 1995). The authors used the ultrasonograph Aloka No 210-DX2 at 3.5 MHz. In larger animals the lateral approach was preferred, due to the presence of ventral osteoderms. EKG: an electrocardiogram was recorded from a 75 cm American alligator. Electrodes applied to the hide did not receive any deections. When pins were inserted into both forelimbs and the left hind limb, deections were recorded, none in lead I, but low deections in leads II and III. The P waves were indistinct and the R wave in lead II measured 2.5 mm. In lead III it was lower and slightly slurred. The T waves were also poorly dened in both leads (Blackford, 1956). Gastric pressure: in chronically cannulated Caiman crocodilus, gastric pressure was recorded with a Beckman Model R Dynograph in relation to temperature and

fasting or feeding (Diefenbach, 1975b). However, this method is beyond the scope of normal clinical examination.

Sample collection Blood Blood can be obtained from several sites: The internal jugular vein runs dorsally within the vertebral column and can best be punctured at the junction of atlas and axis. Flexing the head slightly downwards may help in reaching the vein. Care should be taken not to injure the spinal cord (Olson et al., 1975). The caudal veins run ventrally and dorsally along the vertebral column (ventral and dorsal coccygeal veins). To access the ventral vein, the animal is held in dorsal recumbency. The best place is about onefth of the distance from the cloaca to the tip of the tail. The needle should be long enough and inserted pointing craniad at an angle of 45 from vertical. Bending the tail slightly in the opposite direction helps by opening the space between the long chevron bones covering the haemal canal (Fig. 2.14) (Olson et al., 1975; Gorzula

Fig. 2.14. Taking a blood sample from the ventral tail vein.

Examination of Crocodiles and Clinical Procedures

65

et al., 1976; Samour et al., 1984). The dorsal vein can be reached at a similar distance from the base of the tail, and at a similar angle because of the dorsal spines (Fig. 2.15). This is also the preferred site for a lethal injection. Cardiac puncture: the heart can be found by holding the crocodile lying on its back and observing the slight rise and fall of the ventral wall that accompanies each heart beat (Hopping, 1923). In the American alligator, the heart lies in the midline at the level of the 11th and 12th row of scutes, counting back from the broad band above the forelimbs (Hopping, 1923; Jacobson, 1984). Because of differences in the size of scutes, the number of rows to be counted may differ from species to species. It may, therefore, be necessary to ascertain the hearts exact position by rst examining a dead specimen of the same species. The animal is held in dorsal recumbence and the needle is inserted slowly, until blood is encountered. Small quantities of blood for smears may be obtained by clipping the toe nails, the tips of the tail crests (Olson et al., 1975) or the tip of the tail (Coulson et al., 1950).

TAKING A BLOOD FILM.

A small drop of blood is deposited at one end of a slide and the edge of a second slide or cover slip is dipped into it. The blood is then allowed to spread sideways right across the edge, before the slide or cover slip is pushed along the original slide, thus spreading the blood in a thin, even lm. The frosted edge or the dried blood lm itself can be marked with a pencil (Fig. 2.16). Crocodile red blood cells are nucleated, and these nuclei tend to obscure the stained blood smear if the blood lm is too thick. Therefore, care should be taken to prepare very thin blood lms. The blood lm is allowed to dry in the air. It can be placed face down over two pencils to keep ies away from the blood. When dry, it is xed by immersing it briey in methanol and allowing it to dry again. For the preparation of permanent specimens the blood lm should be stained with Giemsa stain. Urine In the coprodeum the urine is mixed with the faeces, making it impossible to collect clean urine for clinical examination. However, clean urine can be obtained for research purposes by catheterization of the ureters.

Fig. 2.15. Bleeding from the dorsal tail vein.

66

Chapter 2

Fig. 2.16. Preparing a thin blood lm.

Faeces Faeces mixed with urine can be obtained from the cloaca of a crocodile held in dorsal recumbency. They can also be collected from the base of a clean container, in which a small crocodile is kept until it has defecated. For bacteriological sampling of faeces one can simply take a cloacal swab, which is then placed into a sterile container (tube), or a transport medium, and kept refrigerated until it can be examined in the laboratory. Sperm During the breeding season sperm can be obtained by swabbing the seminal groove of the externalized penis. For this the crocodile is immobilized and held in dorsal recumbency (see p. 70). Stomach contents Stomach contents can be sampled by scooping or by washing (Taylor et al., 1978). For

scooping, a piece of rubber-coated metal tube is tied into the opened mouth of the crocodile. A scoop is made from a stainlesssteel or brass rod shaped into a handle, with a loop at a right angle at its end and with a rubber nger, or glove, sewn on to the loop. This is lubricated with vegetable oil and passed through the tube then, with a twisting motion, through the basihyal valve into the oesophagus, and, with another twisting motion, through the pectoral girdle. When it is in the stomach, it can be felt by external palpation and positioned behind a suitable piece of food to be extracted. Throughout this operation the crocodiles head is raised at an angle of about 30 to the axis of the body. Diameters and sizes of tubes and scoops vary with the length of the crocodiles to be sampled. These sizes are shown in Table 2.1. For stomach washing, a clear PVC tube is inserted through the mouth and oesophagus into the stomach. The crocodile is then held with its head above the level of its stomach

Examination of Crocodiles and Clinical Procedures

67

Table 2.1. Dimensions (in centimetres) of crocodiles (Crocodylus porosus) and recommended mouth cylinders, scoops and stomach tubes. The dimensions should be similar for other crocodile species. (After Taylor et al., 1978.) Crocodile length 2835 3550 50120 120130 130140 140180 Cylinder Diameter 3 4.5 5 5 9.5 9.5 Length 2 2.5 3 3 5 5 Scoop diameter Rod Length Diameter Tube Diameter 1 1 1.5 1.5 2 2 Length 40 40 60 60 80 80

2 3 3 4

40 60 60 80

0.2 0.4 0.4 0.4

and water is poured through a funnel into the tube until the abdomen is visibly distended. The abdomen is then squeezed and massaged gently to mix the water with the stomach contents until the water surges up in the tube. The crocodile then is turned with its head down, the free end of the tube is inserted into the collecting bottle and the tube is withdrawn from the mouth of the crocodile. Water and food then ow into the bottle. Three to four washes sufce to clear all the food from the stomach (Taylor et al., 1978). The diameters and lengths of tubes required for the different sizes of crocodiles are shown in Table 2.1. Biopsy Taking samples of diseased tissue from a live animal for laboratory examination may help to establish an accurate diagnosis. The sampling by excision, punches, suction needles or biopsy forceps employs the same techniques as are used in other species (Cooper, 1994).

Solution B Crystal violet Sodium citrate Formaldehyde Distilled water

12.0 mg 3.8 g 0.4 ml 100.0 ml

Haematology Blood sampling has been discussed above (see p. 64). The best diluent for leucocyte and erythrocyte counts for reptiles is Shaws avian solution, which is prepared as follows (Otis, 1974): Solution A Neutral red Sodium chloride Distilled water 25.0 mg 0.9 mg 100.0 ml

Each solution is thoroughly mixed and ltered, then the two are added to each other and mixed again. The stain is now divided into 1.98 ml aliquots and can be kept frozen for up to 3 months. Heparinized blood (20 l) is added to one thawed aliquot and mixed gently for several minutes, resulting in a 1:100 dilution before lling the counting chamber. For the morphology of crocodilian leucocytes see Chapter 1 (p. 24). Haematological values have been reported from several different crocodilian species and are summarized in Tables 2.22.7. Individual and species values vary widely. Runting leads to the depression of many haematological values (Foggin, 1987). White blood cell counts in American alligators infected with Aeromonas hydrophila (see p. 173) increased considerably. In differential counts the heterophils increased from 37.4% to 72.9%, while the lymphocytes decreased from 50.6% to 16.0% (Glassman and Bennett, 1978; Glassman et al., 1981). Infestation of American alligators with the leech Placobdella multilineata (p. 203) resulted in an increase of eosinophils to 60%. After removal of the leeches, the eosinophil levels returned to normal within 6 weeks (Glassman and Bennett, 1978; Glassman et al., 1979). In Nile crocodiles stressed by blasting, the total leucocyte counts decreased, with a relative increase in lymphocytes (Watson, 1990) (see also p. 280).

68

Chapter 2

Table 2.2. Mean haematological values of American alligators. Barnett et al. (1998) 0.67 5.8 9.29 24.4 57.6 11.1 22.3 9.2 1.2 Mateo et al. (1984) 0.38 6.4 Glassman et al. (1981) 0.4 5.3 7.2 18.6 37.4 50.6 3.0 5.5 3.5

Parameter Erythrocytes Leucocytes Haemoglobin Haematocrit Heterophils Lymphocytes Monocytes Eosinophils Basophils

Unit 106 l1 103 l1 g dl1 % % % % % %

54.7 23.9 0.7 10.4 12.7

Table 2.3. Mean haematological values of Caiman latirostris (C.l.) and Caiman crocodilus (C.c.). Parameter Haematocrit Haemoglobin Erythrocytes Leucocytes Lymphocytes Azurophils (?) Monocytes Basophils Eosinophils Heterophils
aTroiano

Unit % g dl 1 106 dl 103 dl % % % % % %

C.l.a 22 9.4 0.56 22.7 65 8 5 1 19 3

C.l.b 19.5

C.c.a 27 12 0.69 16.4 60 9 5 0 21 5

1 1

et al. (1996a); b Tourn et al. (1994).

Table 2.4. Mean haematological values of Crocodylus niloticus (C.n.), C. rhombifer (C.r.) and C. moreletii (C.m.). Parameter Haematocrit Haemoglobin Erythrocytes Leucocytes Neutrophils Lymphocytes Monocytes Eosinophils Basophils Unit % g dl 1 106 l 103 l % % % % % C.n.a 24 7.8 0.60 4.0 6 73 1 2 20?g C.n.b C.r.c 2326 8.18.9 2.42.9 50 21 5 2 22 C.m.d 24.5 7.75 C.n.e 22 7.4 C.r.f 21.7 7.5

1 1

a Makinde and Alemu (1991); b Thurman (1990); c Carmena-Suero et al. (1979); d Sigler (1991); e Foggin (1987); f Moliner et al. (2000a). g Apparently left out of the paper.

Examination of Crocodiles and Clinical Procedures

69

Table 2.5. Mean haematological values of Crocodylus porosus (C.p.) and Tomistoma schlegelii (T.s.). Parameter Haematocrit Haemoglobin Erythrocytes Leucocytes Heterophils Lymphocytes Eosinophils Monocytes Basophils
a

Unit % g dl 1 106 l 103 l % % % % %

C.p.a 19.2 4.9


1 1

C.p.b 24.8

T.s.c 15.2 7.1 0.34 4.35 64.9 24.1 8.5 3.9 0

Wells et al. (1991); b Grigg and Cairncross (1980); c Siruntawineti and Ratanakorn (1994).

Table 2.6. Ranges of haematological values from Crocodylus porosus yearlings (Millan et al., 1997a) and hatchlings (Turton et al., 1997). Parameter Haematocrit Haemoglobin Erythrocytes Leucocytes Heterophils Lymphocytes Monocytes Eosinophils Basophils Thrombocytesa
a

Unit % g dl 1 106 103 103 103 103 103 103 103

Yearlings 1741 4.712.2 0.61.3 6.425.7 0.87.4 4.521.6 0.01.2 0.00.7 0.00.4 471

Hatchlings

l l l l l l l l

1 1 1 1 1 1 1 1

5.33 3.08 1.69 0.05 0.35 0.15

The diagnostic value of thrombocyte counts is still undetermined. In percentage counts they tend to upset the other values.

Table 2.7. Ranges of haematological values from 24-year-old captive Australian crocodiles, four Crocodylus porosus and four Crocodylus johnsoni (Caneld, 1985). Parameter Haematocrit Total plasma protein Erythrocytes Haemoglobin Total leucocytes Thrombocytes Lymphocytes Monocytes Type I granulocytes Type II granulocytes Type III granulocytes Unidentied Unit % gl gl % % % % % % %
1

C. porosus 0.200.22 4870 0.860.98 6277 39.644.2 72.295 0.69 03.0 1.614 00.8 04.8 0.20.8

C. johnsoni 0.180.21 3369 0.710.93 5775 26.448.8 76.587.7 48.5 2.211 38.6 00.5 0.82.8 0.40.8

1012 l
1

109 l

70

Chapter 2

Sexing Crocodiles do not show distinctive sexual bimorphism. American alligators have a differing pattern of scutes around the vent, with three rows of smaller scutes around the vent in males and four rows in females (Viosca, 1939). However, the penis and clitoris of crocodiles of all species and ages differ sufciently in size and shape for an experienced operator to sex even hatchlings with a large measure of condence (Brazaitis, 1969; Whitaker, 1973; Webb et al., 1984). In female hatchlings, the cliteropenis is small with a sharp extremity, while in the male it is large and tubular with a more bulbous extremity (Webb et al., 1984). For the examination of hatchlings, ne curved forceps or haemostats are inserted into the cloaca and spread, thus exposing the cliteropenis which is attached to the cranioventral wall of the cloaca (Webb et al., 1984). In large specimens the index nger is inserted into the cloaca, with the tip of the nger hooked cranially. It is then possible to feel the rigid male organ and to extrude it (Brazaitis, 1969) (see Fig. 1.33).

Cloacal examination As in the case of rectal examination of mammals, larger crocodiles can be examined via the cloaca by inserting a nger into the lower rectum. The animal is held in dorsal recumbency and pressure is applied to the abdomen to shift the organs to be examined towards the midline. In this way intestinal loops and ovarian follicles, as well as hardand soft-shelled eggs in the uterus and vagina, could be identied by palpation in Johnstons crocodiles (Limpus, 1984).

Immobilization When larger crocodiles are to be handled, either for examination and other interventions, or to be moved, the safety of staff has to be considered just as much as the safety of the animal. Being caught and handled is

very stressful for all crocodiles, and this stress can have very deleterious consequences (see p. 278). While there are many instances where crocodiles have been handled and transported safely without chemical immobilization, there are also many cases where the animals have died a few months later from a stress-associated disease. If used at the correct dosage rates and handled properly by competent persons, preferably by veterinarians, immobilizing agents are very safe. The only major cause of mortality encountered in immobilized crocodiles is drowning, which occurs if they are released into water before they have fully recovered from immobilization or if they have been darted in the water (Loveridge, 1979). In this context the recommendation by Flamand et al. (1992) that crocodiles should be allowed access to water once the immobilization is complete is misleading and dangerous. Rather, it should read, once recovery from immobilization is complete (Brisbin, 1966; Loveridge and Blake, 1972; Messel and Stephens, 1980). It should also be noted that the dosages found to be safe and effective in one species may not be so in another (McClure, 1997), for instance, the effective dose of succinylcholine HCl in Crocodylus porosus was ten times that required for Crocodylus johnsoni (Messel and Stephens, 1980). Exploratory trials should always be undertaken and effective doses established before any of these drugs is used on a species for the rst time. These drugs are either given by hand syringe, pole syringe or dart (Flamand et al., 1992). If a hand syringe is to be used, the animal must be restrained beforehand. The preferred sites of injection are the upper foreand hind limbs. The advantages of using these sites are that there are no fat deposits between the limb muscles, which could slow down the resorption of the drug, and that a larger quantity can be injected slowly, thus preventing the liquid from owing out after withdrawal of the needle (Flamand et al., 1992). A pole syringe is safe for the handler, but the injection takes place very rapidly, with the risk of reux through the puncture wound. The preferred injection site is the side of the

Examination of Crocodiles and Clinical Procedures

71

tail, close to its base. If the drug is injected into the fat deposits between the supercial and deep muscles (see p. 29), its resorption will be slow (Flamand et al., 1992). The same site is used for darting, and the same disadvantages apply. In addition there is great danger if the dart should strike an osteoderm obliquely and ricochet off (Flamand et al., 1992). The neck has also been used as a darting site in cases where the darts tended to bounce off the tail (Klide and Klein, 1973). Several drugs, mainly muscle relaxants, have been used for the immobilization of crocodiles. Those that have been reported are shown with their dosage ranges in Tables 2.8 and 2.9. In several species of Crocodylus, gallamine (Flaxedil) has been found to be effective. Its action can be reversed rapidly by the injection of the antidote, neostigmine. While the immobilized crocodiles recover without the help of the antidote, it is essential to have it at hand whenever Flaxedil is used, for the treatment of accidentally injected people (e.g. by a ricocheting dart!). It is also essential to use it when immobilized crocodiles cannot be prevented from entering the water before full recovery. In fact, a large number of transferred Nile crocodiles died on a crocodile farm in South Africa in 1998, when the drugged crocodiles were released into a pen with water, without rst giving

them the antidote. The animals entered the water before having fully recovered and were found drowned the next morning. Many similar incidents have occurred. Recently, exploratory work has been undertaken on the combination of xylazine and ketamine (Seashole et al., 2000). The trial animals were given xylazine 1.5 mg kg 1 body mass and, 20 min later, ketamine 20 mg kg 1 body mass, both injected into the brachial muscles. Immobilization was profound in Crocodylus moreletii and Palaeosuchus palpebrosus, moderate in C. crocodilus, while there was no effect in Palaeosuchus trigonatus. The recommended doses for Flaxedil and neostigmine are given in Table 2.10. However, at the time of writing, Flaxedil has been taken off the market. While it has become available again locally in South Africa, this has opened the quest worldwide for other efcient and safe immobilizing agents for crocodiles. The names of the immobilizing drugs and their synonyms are shown in Table 2.11. The following precautions for crocodile handlers have been suggested by Blake (1993): Do not take chances when working with crocodiles, even small ones. Never work alone with crocodiles. Never use damaged or worn equipment.
1

Table 2.8. Immobilizing agents that have been tried in Alligatorinae (dosages in mg kg Alligator mississippiensis Agent Tricaine Pentobarbitol Etorphine Phenylcyclidine Succinylcholine Diazepam + succinylcholine Dose 8899 7.78.8 0.4 1122 3.05.0 0.220.62 0.140.37 Effect 9h 110 23 h + 67 h 79 h 0.33 3h 35 min 8.8 2.520a 0.5 + Caiman crocodilus Dose Effect

body mass).

Reference 1 2 1 2 3 4 1 1 2 5

+ Effective. Not effective. a Hatchlings. 1, Brisbin (1966); 2, Klide and Klein (1973); 3, Wallach and Hoessle (1970); 4, Hinsch and Gandal (1969); 5, Spiegel et al. (1984).

72

Table 2.9. Immobilizing agents that have been tried in Crocodylinae (dosages in mg kg Crocodylus acutus Agent Succinylcholine Tricaine Phenylcyclidine Gallamine Dose 9.2 Effect 2h Crocodylus palustris Dose 6 Effect 1h 317 * * *

body mass). Crocodylus johnsoni Dose 0.83.6 * * Effect + 0.50.6 0.644.0 11.25 5.0 + + + + Crocodylus niloticus Dose Effect References 1 2 2 2 3 4 5 6 7 2

Crocodylus porosus Dose Effect + +

Chapter 2

Zoletil Suxathonium

* No dose stated. + Effective. Not effective. 1, Klide and Klein (1973); 2, Messels and Stephens (1980); 3, Whitaker and Andrews (1989) (quoted by McClure, 1997); 4, Bonath et al. (1990); 5, Loveridge and Blake (1972); 6, Woodford (1972); 7, Haagner and Reynolds (1992).

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Table 2.10. Recommended doses for Flaxedil and neostigmine in Nile crocodiles (Loveridge and Blake, 1972; Flamand et al., 1992). Weight (kg) Flamand et al. (1992) 2 3 5 8 12 16 21 26 35 55 65 77 95 125 135 165 185 215 230 260 280 295 320 340 350 492 532 Loveridge and Blake (1972) 2 3 5 8 12 16 21 26 35 42 61 77 88 99 108 135 155 179 203 239 297 338 376 415 451 492 532

Length (m) 0.91 1.07 1.22 1.37 1.52 1.68 1.83 1.98 2.13 2.29 2.44 2.59 2.74 2.90 3.05 3.20 3.35 3.51 3.66 3.81 3.96 4.12 4.27 4.42 4.57 4.72 4.88
a b

Flaxedila (ml) 0.10 0.15 0.25 0.40 0.60 0.80 1.50 1.70 2.00 2.50 3.00 3.50 4.00 4.50 5.00 5.50 6.00 6.50 7.00 7.50 8.00 8.50 9.00 9.00 9.50 10.00 10.00

Neostigmineb (ml) 0.05 0.05 0.10 0.20 0.30 0.40 0.50 0.60 0.80 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 2.00 2.00 2.00 2.00 2.00 2.00 2.00

Gallamine triethiodide 40 mg ml 1. Neostigmine methylsulphate 2.5 mg ml 1.

Table 2.11. Names and synonyms of immobilizing drugs as used in the cited literature. Technical Diazepam Etorphine Gallamine triethiodide Phenylcyclidine hydrochloride Sodium pentobarbital Succinylcholine chloride Commercial Valium M99 Flaxedil Sernylan Cap-Chur Barb Anectine, Scoline, Sucostrin Brevidil E MS222 Zoletil

Do not leave drugged crocodiles unattended. Do not forget to remove the tape from the jaws before administering the antidote. Do not allow large, noisy audiences at a crocodile capture exercise. Do not allow the nostrils of the crocodile to be occluded while it is tied up or drugged it will suffocate.

Suxathonium bromide Tricaine methanosulphonate Zolazepam hydrochloride + tiletamine hydrochloride (1:1)

Pre-release screening There is concern about the introduction or spread of diseases where farm-reared, juvenile

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crocodiles are to be released back into the wild. However, habitats already occupied by wild crocodiles usually already harbour all the crocodile-specic pathogens of that species. One should also bear in mind that crocodiles are fortunate in being free from primary pathogens: none of the presently known crocodile-specic contagious agents can be classied as primary pathogens, as they all need triggering factors to precipitate outbreaks of disease. In fact, the presence of these pathogens at a low level in a wild population most likely ensures a state of immunity in the population. For this reason it is possibly not a good idea to release clean juveniles into a new area, not inhabited by crocodiles, as the later introduction of a pathogen might have more serious consequences there. In any case, it is not possible to recommend a programme of rigorous serological screening, as there are no serological tests available for any of the crocodile-specic infections yet, except chlamydiosis. The only recommendation presently possible is to check the condition of the animals to be released, and only release healthy looking, well-nourished individuals, originating from a farm where no undue mortality has occurred in the preceding 12 months. The presently known crocodile-specic pathogens are: crocodile poxvirus (p. 158); caiman poxvirus (p. 157); adenovirus (p. 160); Mycoplasma spp. (p. 167); Chlamydia sp. (p. 167); coccidia (as yet unnamed) (p. 183).

Tagging and identication Natural markings For many purposes it is useful to be able to recognize or mark individual animals. Nile crocodiles have dark spots on the sides of their tail which vary individually. Swanepoel (1996) used the markings on the last nine tail segments with horizontal scutes that precede the segment with the rst single vertical scute (Fig. 2.17) on both sides of the tail (R and L). By numbering the segments 19 from caudal to cranial, and by recording the segments with markings, doubling the number for double markings, a code could be established. This could be further rened by distinguishing between black and grey markings, placing the code numbers for grey spots in brackets, and by adding a sketch of the side view to the record. Using nine rows of scales on either side of the tail of almost 300 crocodiles, Swanepoel (1996) found an accuracy of 95%. The degree of accuracy could be increased by using ten or even 12 rows. This method is applicable to wild populations as well as to farmed animals, e.g. in a breeding colony, and could also be applied to other species of crocodiles.

Clipping Several ways of marking crocodilians have been used. Toe clipping limits the number of individuals that can be marked, and the accidental amputation of a toe as a result of biting or ghting is quite common (Dixon and Yanowsky, 1993). Clipping the dorsal crest of the tail is difcult, if not impossible in hatchlings. As the marked individuals grow, the mark becomes smaller in relation to the overall size of the animal (Dixon and Yanowsky, 1993). Tags Web-tagging has been used widely, but tags are frequently lost, and limbs are also lost occasionally leading to the loss of a record (Dixon and Yanowsky, 1993). Tags applied to one of the dorsal crests in adult crocodilians are often used. However, they occasionally

The only other pathogen that one should possibly consider is Mycobacterium avium (p. 170), which could be perpetuated in a wild population through cannibalism. However, this pathogen does occur in wild birds and has recently been involved in mass mortality in amingos in Kenya (Kock et al., 1999). There may perhaps be a difference in pathogenicity for crocodiles between M. avium strains originating from pigs and those from birds. The mycobacteria may also need stress or other triggering factors to cause disease.

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Fig. 2.17. Spots on the tail of a Nile crocodile used for identication (after Swanepoel, 1996). Reading from caudal to cranial, this crocodile would have the code R113346688.

get lost, and the numbers are not easy to read (Dixon and Yanowsky, 1993). On South African crocodile farms the colour of these tags is used to indicate the sex of the animal. None of these markings is acceptable for zoos and other tourist exhibits. Microchips Transponder chips or microchips have been used successfully in broad-snouted caimans (Dixon and Yanowsky, 1993). The chips were inserted into the left side of the tail base, and it was found that the microchips did not migrate from the site of implantation, nor was there any scarring of the skin. A serious disadvantage of this method is the fact that the reading device only works from a maximum distance of about 20 cm, forcing the operator to come dangerously near to the animal to read it, or to capture and restrain the animal rst. The presence of the chip in the tail meat may also affect its acceptability in certain countries. Since 1997, the European community has required all crocodilians to be microchipped (as are all Annex A listed vertebrates) if used for commercial purposes such as sale, display, breeding, etc. (Redrobe et al., 1999). The British Veterinary Zoological Society advises

injection of the microchip in crocodilians dorsally into the neck, anterior to the nuchal cluster (Redrobe et al., 1999).

Post-mortem Examination
Storage and transport of the carcass Dead crocodiles are usually found in a very warm environment and, at that temperature, tend to decompose very rapidly. Therefore, it is important to collect the dead animal as soon after death as possible and cool it down to about 410C. Larger bodies cool more quickly if immersed in ice water. Freezing a carcass should be avoided as the formation of ice crystals destroys the cells and renders the carcass unsuitable for histopathological examination. However, when refrigerated, psychrophilic bacteria continue to multiply and may overgrow those pathogens potentially involved in causing the mortality. Thus freezing a few specimens purely to maintain the microbial ora for examination in the laboratory might be considered. In any case, the carcass should be taken to a diagnostic laboratory as soon as possible remember that laboratory procedures also cause delays and that the usefulness of a

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diagnosis decreases with the time lapsed after the death of the animal. The laboratory should be alerted and the carcass transported to the laboratory, size permitting, in an insulated container and on ice. The cost of an examination and investigation is usually small compared with the value of the animals lost. If there is a high mortality, several carcasses should be submitted, but a whole bagful of dead hatchlings may only tire the pathologist without contributing to the eventual diagnosis. At the laboratory the pathologist should be given as complete a history as possible, including the age and number of animals affected, and be provided with contact numbers (phone, fax and e-mail) and address. Most laboratories have forms for this purpose.

immediately ready for further procedures. The spot to aim at is in the middle, between the orbits and the supertemporal fossae (Fig. 2.18). Small specimens can be given a lethal injection of a barbiturate either intraperitoneally (see p. 89), into the heart, the dorsal neck vein (see p. 64) or into the dorsal or ventral tail vein (Figs 2.14 and 2.15). Catto and Amato (1994b) used intracerebral injections of ethyl alcohol, but the route of injection and dosage rate were not given, nor did the authors comment on the effectiveness of this method.

Examination of head and skin Before opening the carcass, the head and skin are examined. The examination of the head includes the eyes (eyelids, nictitating membrane, cornea), the nostrils and the mouth (gingivae, teeth, tongue and gular valve). The skin of the whole body is checked for injuries, ulcers, swellings, abrasions (under the chin and the soles of the feet, see p. 242), pox (pp. 157 and 158) or pox-like lesions (p. 236) and any other abnormalities. Then the total length is measured, recorded and, if possible, the animal is weighed.

Humane killing Live specimens that have been submitted for post-mortem examination will have to be put down humanely. Larger crocodiles (>60 cm) are killed easily with a captive bolt stunning gun, as used for the slaughter of pigs or cattle. This destroys the brain of the crocodile completely, rendering the animal

Fig. 2.18. Head of a farmed Nile crocodile killed with a captive bolt stunning gun. The correct spot to aim at is in the centre, between the orbits and the supertemporal fossae.

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Opening the carcass The animal is placed on the table with its belly up and the skin is incised across the lower neck, just cranial to the row of large scales between the fore limbs (Fig. 2.19). From there the skin and body wall are cut along both sides of the body, rst through the coracoid and then through the cartilaginous part of the ribs. The coracoids are very tough, and in adult animals it may be easier to cut through their cartilaginous junction, in the midline, before going to the ribs on either side. In larger specimens the skin is taken off prior to the removal of the ventral body wall (Fig. 2.20). The lateral cuts are continued beyond the ribs through the abdominal wall, taking care not to cut into any of the abdominal organs, particularly into the stomach which is attached to the left body wall. The pubic bone protrudes cranially from the pelvic girdle. In hatchlings it can be removed with a transverse cut, in older specimens it becomes extremely tough and can be left in place and the transverse cut made just cranially to it. The skin with the ventral body wall is now lifted and all adhesions are carefully dissected until the whole piece can be lifted off, exposing the thoracic and some of the abdominal organs (Fig. 2.21).

Neck, pharynx and oral cavity The lateral cuts are continued in a cranial direction to the maxillary joints, and then medially of the mandibles to the tip of the tongue. This ap of skin with the tongue is lifted off, exposing the hard and soft palate, with the dorsal ap of the gular valve, the internal nares, the ventral opening of the Eustachian tubes and the larynx (Plate 5) (see p. 11). Along both sides of the neck it may be possible to see the chains of thymus glands (p. 21). However, they are no longer present in emaciated animals.

Examination of the thoracic viscera The thoracic part of the trachea is inspected rst. Then the various thoracic endocrine glands are located, which may be hidden in fat deposits: the multiple lobes of the thymus gland, the thyroid(s) and the parathyroids (see p. 22) (see Plate 3). The pericardial sac is opened, the heart is taken out, and the auricles separated from the ventricles. Note that crocodiles do not have fat in the coronary groove. The two lungs are then loosened from their attachments to the body wall and the prehepatic

Fig. 2.19. Line of incision across the lower neck and along the sides.

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Chapter 2

Fig. 2.20. In larger specimens the ventral skin is taken off before removal of the ventral body wall.

Fig. 2.21. Opened carcass with the ventral body wall deected caudally.

transverse membrane. These attachments are normal, but they vary in extent from species to species. The lungs can then be taken out for closer examination. This leaves the oesophagus, which is situated in the mediastinum and is attached dorsally to the body wall.

Examination of the abdominal viscera Before fully exposing the abdominal viscera it may be necessary to carefully remove the ventral diaphragmatic muscle, which runs from the cranial transversal membrane to the pubic bone. Its removal exposes the two

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lobes of the liver, the stomach on the left side, the fat body on the right side and a few intestinal loops (Fig. 2.22). The duodenum is severed where it emerges from the pyloric antrum of the stomach, and the whole intestine is gently pulled loose from the mesentery and lifted out to the left side of the body. The fat body is then lifted out, giving access to the spleen dorsally in the mesentery (Fig. 2.23). The size of the fat body is a better indicator of the actual state of nutrition than any subperitoneal fat that may be present, as such fat is poorly metabolized, while the fat body is a very active fat storage organ, supplying the daily needs, particularly of the heart (see p. 28). Cranially the spleen is surrounded by the caudal pancreas, the cranial pancreas is found between the duodenal loops. The spleen is covered by a very strong brous membrane, which normally grows as the spleen itself grows but does not stretch when the spleen hypertrophies in response to an infection. In such cases, the spleen tissue buds through the capsule. Such a budding spleen is a clear sign of hypertrophy splenomegaly, indicating infection and septicaemia (Fig. 1.46) (Huchzermeyer, 1994). The stomach is severed from its attachment

to the left body wall and then lifted out with parts of the oesophagus. It is then opened and inspected for normal contents, foreign bodies (p. 254), parasites (pp. 192 and 194) and ulcers (p. 251). Next, the two lobes of the liver, together with the gall bladder, can be removed and examined. The intestine is then cut off at its most caudal accessible end. It is opened for closer examination, at least in parts. It is now possible to attempt a cut through the pubic bone towards the cloaca and excise the cloaca. This leaves the gonads partially covering the adrenals, the Muellerian ducts or the oviducts and nally the kidneys, attached to either side of the backbone in the caudal recesses of the abdominal cavity.

Tail, legs and feet The tail is cut across, not far from its base, to expose the fat deposits between the supercial and deep muscles (p. 10). The legs and the joints are examined for any swellings and, if necessary, the joints are opened to examine them for arthritis (p. 273) and gout (pp. 230 and 264) (Fig. 2.24). Any other swellings are also incised and examined.

Fig. 2.22. Abdominal organs exposed after removal of the diaphragmatic muscle: a, liver; b, stomach; c, fat body; d, duodenal loop; e, loops of jejunum and ileum.

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Fig. 2.23. The spleen in situ dorsally in the mesentery, cranially surrounded by the caudal pancreas.

Fig. 2.24. Opened carpal joint.

Brain and spinal cord In smaller specimens (<1.5 m) the skull can be split longitudinally in the midline from the ventral aspect (the head upside down) with the help of a strong knife and a hammer (Fig. 2.25). This gives access to the nasal cavi-

ties and both halves of the brain (Fig. 2.26). For mature specimens a saw has to be used to open the skull. Sections of the vertebral column can also be opened longitudinally with a knife and hammer, to expose the spinal cord. I have never been able to pull the spinal cord as is

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Fig. 2.25. Splitting the skull of a juvenile Nile crocodile from the ventral aspect with a strong knife and a hammer.

Fig. 2.26. The split skull, exposing the nasal passages, the halves of the brain and the pituitary gland (p. 21) at the base of the brain (arrow).

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done with slaughtered dwarf crocodiles in the Congo Republic. There, the butcher ladies at the markets cut dorsally through the neck down to the vertebral column, bend the head down and grip the spinal cord between two ngers before severing it cranially. Then, while gently tapping the back with the blunt side of the machete, they slowly pull out the entire spinal cord (Fig. 2.27). They claim that the meat is inedible if the black worm is left inside. Sample collection Blood If the animal is still alive, blood samples can be collected as explained above (p. 64). During post-mortem examination, blood can be collected from the auricles of the heart. Note, though, that the cells deteriorate after death, and that only the freshest carcasses will have blood that is still suitable for some of the laboratory tests. The method for the preparation of thin blood smears has been explained above (p. 65). The blood smears are air dried and then xed by immersing them in methanol, or by letting methanol run over them. They are air dried again, and can

then be wrapped in tissue paper or placed in a container for dispatch to a laboratory. Bacteriology Samples for the isolation of bacteria should be taken with sterile instruments before the organs have been contaminated by handling, and should be placed in sterile containers. If they cannot be delivered to the laboratory immediately, they should preferably be frozen to prevent any further growth by contaminating bacteria. If sterilized instruments are not available, scissors and forceps can be immersed in a 10% formalin solution, such as is used for the preservation of histopathology specimens (see below). In the case of a generalized infection, all internal organs will contain the bacteria, as crocodiles have no lymph nodes and are therefore unable to localize an infection in a particular organ system. Therefore it is unnecessary to collect bacteriological specimens from all the organs, normally the liver sufces. In addition, one should sample specic lesions or organs that are visibly diseased. In cases of enteritis, either a piece of unopened intestine is collected or a small quantity of intestinal contents. The organ

Fig. 2.27. Pulling the spinal cord from a slaughtered wild-caught African dwarf crocodile at a market in Brazzaville.

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samples should be taken in the form of small cubes, with a side length of 510 mm, and placed in separate containers. Viral isolation If a viral infection is suspected, rst discuss with staff at the virology laboratory whether such a virus can be isolated at all (see p. 157). An alternative may be to demonstrate virus particles in uids (intestinal contents) by negative staining and transmission electron microscopy (TEM) (Huchzermeyer et al., 1994b). Virus particles can also be detected by TEM in tissues that have been xed in glutaraldehyde solution. The details would have to be discussed with the electron microscopist at the laboratory. Some viruses cause the formation of typical inclusion bodies, which are detected by histopathological examination (see below). Histopathology For histopathological examination, small cubes of tissue (510 mm side length) should be placed in 10% formalin solution. Formalin is normally sold as a 40% formaldehyde solution, which is regarded as 100% formalin (saturated solution). One part of this, diluted in nine parts of water gives the 10% formalin solution that is required. Laboratories prefer to dilute the formalin in buffered distilled water or in buffered saline solution. However, in an emergency, sufciently good results can be obtained by using tap water as diluent. Note that the formalin becomes further diluted by the water in the tissues. Therefore, it is advisible to immerse the tissue cubes in about ten times more formalin solution than the actual mass of the tissues to be preserved (e.g. 10 g of tissues in 100 ml of solution). Formalin penetrates the tissues only very slowly, and this causes large pieces to rot inside while only the outer layers are xed by the preservative, particularly under warm or hot climatic conditions. This is the main reason why small cubes of tissue should be used. It is wise to collect tissues from all organs and from all the different lesions encountered, but tissues from different animals

should be kept in separate containers. The histopathologist can then choose which organs to examine in each particular case. By limiting the number of organs collected, the ability of the pathologist to establish the correct diagnosis is also limited. Parasites Stomach and intestine are cut open in their whole length and placed in a screw-cap jar, which is lled to one half with water. The cap is tightened and the jar shaken vigorously. Then the contents are poured through a strainer (coffee strainer) and the contents of the strainer washed out into a dark plastic tray, in which the parasites can be found. Intestines from very large crocodiles may have to be processed in smaller sections. Parasites are best preserved in 70% ethyl alcohol. Roundworms tend to roll up into tight balls when placed in alcohol. They are then difcult to examine later under the microscope. It is better to place them in a test tube with saline solution, or even tap water, which is then heated over a ame to almost boiling. At that moment the parasite stretches out, and it remains stretched when placed in alcohol.

Collecting specimens in the eld Required material Field work often takes place far away from the nearest laboratory, under difcult climatic conditions and usually also with severe restrictions regarding space and weight allowed for equipment and materials. The minimal requirements comprise the following instruments: a knife; scissors (both good quality and sharp); forceps and razor blades; a number of very small (25 ml) and small (2030 ml) plastic screw-cap jars; a few larger (200 ml) screw-cap jars; one 500 ml screw-cap jar; a few 10 ml plastic syringes with needles; two test tubes;

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glass slides and cover slips; a coffee strainer; a small cutting plank; a plastic tray; a plastic measuring cylinder (250 ml); 500 ml of formalin (40% formaldehyde solution see above, p. 83), 500 ml of 70% ethanol and 500 ml of methanol, all three in sturdy plastic cool drink bottles; a few similar spare bottles for the solutions to be made up, and; an insulated box for the transport of frozen specimens. Also required are masking tape, a roll of toilet paper, a pencil, paper and a marking pen. Bacteriology and blood samples If there is no access to a freezer, bacteriological and serum samples cannot be taken. If a freezer is available, the bacteriological samples are taken as explained on p. 82, but in the smallest possible containers, marked on the outside with the specimen number and placed in the freezer as soon as possible. For serum samples, the blood is collected from the auricles, one drop of blood is placed on a glass slide for a blood smear (see p. 65) and the rest squirted gently into a 20 ml jar, marked on the outside and placed on its side in the shade, but not refrigerated, to allow the blood to coagulate in a slope (Fig. 2.28). Once the blood has coagulated, the jar is stood

upright again to allow the serum to collect at the bottom. After a few hours, the serum can be drawn off with a syringe and needle, squirted into a very small jar, marked on the outside again and placed in the freezer. The air-dried blood smears are marked with a pencil, either on the frosted end or on the thicker part of the smear. After xing and drying they can be rolled into a short length of toilet paper (Fig. 2.29) and secured tightly with masking tape. Several blood smears rolled up tightly in toilet paper are fairly well protected from breakage.

Histopathology samples A 1:10 formalin solution is prepared with either tap or other drinking-quality water, using the measuring cylinder, and poured into one of the spare bottles. One of the 200 ml jars is roughly half-lled from this stock for the initial xing of the histopathology samples, which are cut as small as possible and left in this jar for 2448 h without refrigeration. The specimen number is written, with a pencil, on a small square of paper, and also placed into the jar. After 1 or 2 days of xing, the contents of the jar are poured through the coffee strainer into a second jar. The xed organ pieces are then placed into the plastic tray and are trimmed with a razor blade on the small cutting plank to the minimum size required for embedding (usually

Fig. 2.28. Jars lying on their side to allow the blood to coagulate in a slope.

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Fig. 2.29. Several blood smears wrapped tightly in toilet paper are fairly secure from breakage.

writing in pencil on paper is not washed off by immersion in the liquid, while glued-on labels or writing with a marker pen easily come off if there is an accidental leak. Pentastomes (p. 205) are collected by deeply incising the lungs. If the parasites are still alive, they will come out into the air and can then be picked up easily. For a thorough search, the lungs should be cut into small pieces, washed in the 500 ml jar and the contents then examined in the tray. These are the absolute minimal requirements for the collection of standard specimens, tried on several Congo expeditions. If you can carry more, do so by all means. If there are any specic requirements, e.g. samples for toxicological investigations, you should ask the laboratory for detailed instructions.

3 mm thick pieces, about 5 10 mm wide and long, for details consult a pathologist). These pieces, together with the square of paper, now t into one of the small jars, in which they are covered with some recycled formalin. They are now ready for storing at ambient temperature and eventual transport back to the laboratory. Do not refrigerate samples in formalin! If necessary, the remainder of the formalin can be used a second time for xing another set of specimens. Parasites Stomach parasites can be picked directly out of the opened stomach, or the stomach contents can be poured out into the plastic tray in which the parasites become more visible. The intestine is cut open along its whole length and placed into the 500 ml jar. This is roughly half-lled with water, the cap is closed and the jar is shaken vigorously. The intestine is then taken out and the remaining contents of the jar poured through the coffee strainer. The contents of the strainer are then washed with a small amount of water into the tray, where the parasites can be collected. Fixation of the parasites with heat and in alcohol has been explained above (p. 83). For storing the parasites, use the smallest possible container and place a square of paper with the pencilled specimen number in the jar with the sample. Store at ambient temperature. Note that

Age determination Crocodiles do not have any outwardly visible markers that can be used to determine their age. Their growth also varies individually, for example runted 1-year-old yearlings can be the same size as 1-month-old hatchlings. Unless the date of hatch is known and stated, one should not attempt to guess a crocodiles age, but rather record its length and weight. Crocodiles that are exposed to hot and cold seasons, as a rule, grow faster in the hot than in the cold season. In such crocodiles the bone is deposited in laminae of varying thickness, similar to tree rings. These bone rings can be visualized and counted in histological preparations (de Buffrnil, 1980a,b; de Buffrnil and Buffetaud, 1981; Hutton, 1986).

Organ morphometry In animals with very large variations in overall body size, it is often difcult to judge the relative size of a particular organ in an individual case. However, for a pathological diagnosis it is important to be able to determine whether an organ is hypotrophic, hypertrophic or normal. Huchzermeyer

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(1994) found a close relation in Nile crocodiles between the mass of the two ventricles of the heart (total ventricular mass, TV) and total body length, so TV is used as the standard against which the other organs are measured (Fig. 2.30). To make this comparison, the organ in question is weighed and so is the heart, without the auricles. The weight of the organ is then divided by the weight of the ventricles, resulting in the following ratios: spleen :heart ratio (SHR); fat body :heart ratio (FHR); kidney :heart ratio (KHR). The spleen :heart ratio indicates the state of activity of the spleen. The SHRs of normal and diseased Nile crocodiles are shown in Table 2.12. It must be borne in mind, though, that often the affected crocodiles die very slowly, and that after a long illness the spleen becomes hypotrophic again and could appear normal. The fat body :heart ratio indicates the actual state of nutrition. An FRH <0.5 indicates an animal in a very poor state, while an FRH >5 indicates an overfed animal (excess energy). The kidney:heart ratio was found to be of limited use, as there was little variation in relative kidney mass and visibly affected kidneys could be detected without weighing.

Examination of unhatched eggs On farms where poor hatching results are obtained, it may be necessary to open and examine all unhatched eggs, particularly those from nests with very poor results. If the eggs are to be submitted to a laboratory, they should be kept refrigerated, but not frozen, before and during transport. The eggs are cut open lengthwise with a small pair of scissors and the contents poured into a dish. After each egg has been examined, the contents of the dish are poured into a bucket for eventual disposal. Infertile eggs usually remain clear throughout the incubation period and no sign of banding or remains of an embryo can be found. If any contamination has penetrated into the egg, the contents become putrid, and in such an egg a small, dead embryo may have dissolved altogether. Consequently an infertile egg may be difcult to differentiate from one with early embryonic death. A microsatellite analysis procedure, based on parental DNA, has been described for the exact differentiation between infertile eggs and early embryonic death, but may not be applicable to routine farm investigations (Rotstein et al., 2002). Larger embryos can, however, be found and examined. From their state of development one can try to judge at which point during incubation the embryo has died. If contamination is found, or is suspected to be the problem, submit some swabs to a bacteriology laboratory (i.e. sterile swabs dipped into the liquid before it has been poured out of the egg).

Medication
Administration of medication Mass medication Mass medication is rarely given in the water, as only a small part of the water is consumed by the crocodiles. Medication of the water is suitable for the external treatment of skin infections and for a supportive treatment with salt (1 g l 1). The salt is intended to

Fig. 2.30. The relative sizes of myocardium, fat body and spleen.

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Table 2.12. Spleen : heart ratios (SHR) of Nile crocodiles in relation to different pathological conditions (Huchzermeyer, 1994). SHR values indicate the degree of splenomegaly. Condition No apparent infection Conjunctivitis, mostly chlamydial Septicaemia Salmonellosis Gastritis Enteritis n, Number of cases. Range 0.190.72 0.112.12 0.242.57 0.222.68 0.412.49 0.342.71 n 77 40 84 70 54 35 See also Chapter 5, p. 167; Chapter 7, p. 245 Chapter 5, p. 173; Chapter 6, p. 228 Chapter 5, p. 164 Chapter 7, p. 251 Chapter 6, p. 226; Chapter 7, p. 255

replace salt lost into the fresh water by animals that have not eaten for a while, and thus have not been able to obtain salt from their food (see pp. 41 and 282). Antibacterials and anticoccidials can be administered via the food. Medicated pelleted rations will have to be prepared specially for the purpose. When medication is to be incorporated into wet rations based on meat or sh, only one-quarter of the dry ration dose should be used to compensate for the high moisture content of the ration. Mixing powders or liquids accurately into wet rations is extremely difcult and an even distribution of the medication is rarely achieved. If the mince is spread out in a thin layer on a tray, a liquid can be sprayed over it. Medication in powder form should rst be mixed into bonemeal to increase its bulk, and only then be mixed into the mince. Individual dosing Small crocodiles that can be handled easily (hatchlings) can be dosed individually by mouth, in the following way. The liquid (0.20.5 ml) is drawn into a 1 ml plastic syringe. The crocodile is held in one hand, with the thumb and index nger holding the base of the mandible (Fig. 2.31). Tapping the hatchlings nose lightly with a pen causes it to open its mouth, or the mouth is forced open gently with the tip of a nger of the other hand, and the entire syringe is slowly pushed into the mouth, past the gular valve and into the oesophagus, to the cardia of the stomach. Then the plunger is pushed down before the

syringe is withdrawn slowly. The crocodile is still held upright for a while, so that the liquid is not regurgitated. During the whole procedure care should be taken not to exert any pressure on the stomach. Larger crocodiles can be force-fed by stomach tube in the same way as for collecting stomach contents (see p. 66). It may be easier to use a exible tube, threading it through a hole of appropriate size drilled through a long piece of wood, which can be held still by an assistant (Fig. 2.32). The method described for stomach washing (p. 66) can also be used for force-feeding. Larger, even very large crocodiles, particularly ones that have not eaten for a long time and need dosing with sugar to stimulate their hunger, can be dosed with a thick sugar syrup (e.g. treacle or honey), which can also be medicated with whatever is required. The syrup is rolled on to one end of a long stick (broomstick), and with another stick or plastic pipe the crocodile is tapped on its snout until it opens its mouth. The syrup then is slapped into the back of its mouth and wiped off on the tongue. From there it will be swallowed slowly by the crocodile. After dosing, the crocodile should be prevented from entering the water, so as not to wash the syrup out of its mouth (personal communication, P. Martelli, Singapore, 1994). Injections The resorption of injected medication is slower in reptiles than in mammals or birds because of the slower heart rate (p. 43). It is

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Fig. 2.31. Dosing a hatchling with the help of a 1 ml syringe.

Fig. 2.32. Dosing by stomach tube.

also temperature dependent slower at lower, and faster at higher temperatures. It is recommended not to inject oily solutions or emulsions, as their resorption is even slower (Kraft,

1978). Oils and emulsions may also elicit a local inammatory response, and the exudation of brin may prevent the resorption of the injected substance entirely (see p. 46).

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89

Because of the tight adherence of the skin and the many cutaneous muscles, it is hardly possible to give subcutaneous (sc) injections to crocodiles, except under the ventral skin, which is less accessible. When giving intramuscular (im) injections, one should try to avoid injecting into accumulations of body fat, which would slow down the resorption. This often happens with deep injections into the tail. The ideal sites for im injections are the muscles of the upper limbs. An injection with a pole syringe is best given caudolaterally into the junction of hind leg and tail. Intraperitoneal (ip) injections are given either in the ventral midline, cranial to the pubic bone, in small crocodiles that can be held in a belly-up position, or, in larger specimens, laterally on the right-hand side cranial to the knee. It is also possible to inject into masses of fat here, with a consequently reduced speed of resorption. The sites for intravenous (iv) injections are the same as those that are used for taking blood samples (see p. 64). However, it should be noted that all these sites only allow the needle to be placed in a perpendicular position to the vein and, therefore, some or even all of the liquid could well be injected paravenously, particularly if the animal struggles during the injection. A case of paravenous injection during an attempted blood transfusion into the supervertebral (internal jugular) vein in an African dwarf crocodile ended in the death of the crocodile due to compression of the spinal cord by blood entering the subarachnoid space (Heard et al., 1988). For future attempts of blood transfusion, the authors recommended using the tail veins, or the external jugular vein after surgical dissection. Tibial puncture An alternative to the iv route may be tibial puncture in the middle of the proximal third of the tibia. This allows the needle to be placed in the venous sinuses in the head of the tibia. The injected liquid will be transported very rapidly from this site. This may be the route of choice when a needle must be left in place for repeated injections or blood sampling, e.g. for pharmacokinetic studies. This method has

been adapted from paediatrics and has been used successfully in birds (Ritchie et al., 1990).

Drugs and dosages Generally, the same drugs that are used in poultry can be used in crocodiles. For a single dose, the same dosage should be used as in poultry. However, excretion is generally slower in crocodiles and, therefore, repeated administrations should be spaced accordingly. Normally, with drugs being given in the food, this evens out, as crocodiles tend to eat only every second day. The dosage should also take into account the relatively low feed intake of crocodiles. The dosage levels given in Table 2.13 have been calculated for the average feed intake. Another point to be taken into consideration with mass administration of medication is the possible effect on the environment. Many drugs are excreted unaltered and will be washed out with the water. They have the potential to pollute rivers or other natural water bodies into which the efuent from the crocodile farm is released. Some of the metabolites of commonly used drugs are also biologically active. The antibiotic sensitivity of bacteria isolated from crocodiles varies considerably. It is therefore recommended that antibacterials should be used only after the sensitivity of the bacteria in question has been established in a laboratory (see p. 91). The prolonged or repeated prophylactic use of antibiotics only serves to increase the level of resistance in all the bacteria exposed to the particular antibiotic. This resistance can even be passed on to other species of bacteria, creating problems when the same antibiotic could, or should, be used in a disease outbreak. This is the reason why the prophylactic use of antibiotics should be strictly avoided (see also p. 91). The commonly used drugs and their dosages have been collated in Table 2.13. Note that ivermectin is toxic to crocodiles (see p. 225). It causes paralysis when used at half the mammalian dose (personal communication, C.M. Foggin, Harare, 2000).

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Table 2.13. Drugs and dosages commonly used in crocodiles. Drug Tetracyclinea 10 mg kg Tetracycline long actinga Kanamycina Gentamycina
1

By mouth

im 75 mg kg 10 mg kg 20 mg kg 20 mg kg 2.5mg kg 3 mg kg
1

In feed 1.5 g kg
1 1

Times Single dose Daily for 10 days Daily for 9 days For 410 days Repeat after 3 days Every 2nd day for 8 days Every 3rd day for 15 days 2 per day for 9 days Daily for 4 days Repeat after 2 days For 5 days

Refs 1 1 3, 4 5 5 2 3, 4 5 3, 4 5 5 6 5 5 5 5 5 5 3, 4 5 5 4 4 4 5 7 6

0.5 g kg
1 1

Chloramphenicola

20 mg kg

1030 mg kg Penicillinsa Danooxacin (Advocin)b Enrooxacin (Baytril)b Sulphachloropyrazine (ESB3)b Amproliumb Toltrazuril (Baycox)b Ketaconazolea Fenbendazole (100 mg ml 1) Oxfendazole (22.6 mg ml 1) Thiabendazolea Mebendazolea Piperazinea Ca-borogluconate (250 mg ml 1) Doramectin 1% NaCl
a

0.1 MIU kg

1 g kg 0.050.2 ml kg dilute 1:5, 5 ml kg 1 10 g kg 2 g kg 1 g kg 7 ml kg 50 mg kg


1 1

1 1 1 1

2 ml kg 5 ml kg 50 mg kg 20 mg kg 50 mg kg
1

For 4 days Daily for 7 days Continuously For 3 days 1 repeat after 2 weeks For 3 days For 3 days 1 repeat after 2 weeks 1 repeat after 2 weeks 1 repeat after 2 weeks

ip, dilute 1:2, 3 ml kg 1 1 ml 50 kg 1 In water 1gl 1 For 10 days

Active substance. As product. 1, Huchzermeyer et al. (1994a); 2, Huchzermeyer (1991a); 3, Verseput (1986); 4, Jacobson et al. (1983); 5, Foggin (1992a); 6, own recommendation; 7, C.M. Foggin, Harare (2000), personal communication.

Vaccines Vaccines are used to stimulate antibody production against specic pathogens. For the preparation of such vaccines it is necessary to culture and propagate the specic disease agents. Few vaccines have been used in crocodiles so far, as none of the crocodile-specic

viruses have yet been cultured. In an inactivated vaccine, the agent has been killed to prevent its further multiplication and spread, while a live vaccine allows the agent to multiply in the inoculated host. An autogenous crocodile pox vaccine was prepared and tested successfully by Horner (1988a). He macerated 1 g of pox crusts,

Examination of Crocodiles and Clinical Procedures

91

collected from the skin of affected crocodiles, in 10 ml of phosphate buffered saline, added 1 MIU penicillin and 1 g streptomycin, and left the suspension standing for 24 h, after which it was centrifuged at 180 g for 10 min. The trial hatchlings were inoculated with 0.5 ml of this vaccine sc between the hind leg and the base of the tail. Mohan et al. (1997) reported the vaccination of Nile crocodiles against Mycoplasma crocodyli. The vaccine was inactivated with formalin, and contained aluminium potassium sulphate as an adjuvant. The use of an inactivated calf paratyphoid vaccine as part of a range of therapeutic and preventive measures in an outbreak of salmonellosis in farmed Nile crocodile hatchlings was reported by Huchzermeyer (1991a).

few hours. A second state of shock occurred more than a day later, and was due to hypoglycaemia. Large amounts of glucose promoted the formation of liver and body glycogen. For 2 h after the injection of adrenaline no effects on blood glucose or pupillary response were observed. After 2 h the pupils contracted to slits and blood glucose rose by several hundred mg ml 1. Adrenaline reduced the glycogen stores of the liver to about one-third and the body glycogen to about one-half of normal values within 24 h. Prolonged daily injections of cortisone, 10 mg kg 1 body mass, caused a moderate hyperglycaemia. Daily injections of ACTH, 5 mg kg 1 body mass, had no effect.

Antibiotic resistance The antibiotic resistance of pathogenic bacteria depends on previous exposure to these substances. If crocodiles are fed the meat or whole carcases of farm mortalities, they acquire the pathogens of these animals, which will be resistant to any antibiotics to which they have been exposed previously. This is the case particularly if poultry or pigs are used as crocodile feed. As not all bacteria are killed during a course of treatment, the most resistant ones are likely to remain alive and pass on their genes for resistance to their progeny. Bacteria can also transfer these genes to other bacterial species, thereby causing a whole population of bacteria to become resistant very rapidly. Continuous use of antibacterials on the crocodiles themselves can obviously also stimulate antibiotic resistance and should therefore be avoided (see above).

Pharmacokinetics Pharmacokinetics deals with the fate of drugs in the body, their absorption, distribution, metabolization and, nally, their excretion. Hardly any work has been carried out in this eld in crocodiles. We assume that, because of the slow circulation in crocodiles, the resorption, distribution and excretion of any drug are much slower than in birds and mammals, and that they are temperature dependent. We also assume that, because of the low metabolic rate of crocodiles, they are metabolized more slowly. Drug dosage rates (p. 89) have generally been calculated on the basis of these assumptions, and in certain cases have been corrected if and when signs of toxic effects occurred. There is no doubt that species differences might occur among the crocodilians regarding pharmacokinetics and drug tolerance. This is a very wide eld of research that urgently needs attention. In this context, the paper by Coulson and Hernandez (1953), regarding glucose, insulin, adrenaline and ACTH in the American alligator, deserves particular mention. The authors found that injected glucose is removed from the bloodstream at a very slow rate. One unit of insulin per 1 g of body mass produced an immediate state of shock due to hyperglycaemia, which lasted for a

Surgical Interventions
Most of the procedures described in the following were designed for experimental surgery, used in physiology research. In cases in which clinical surgery becomes necessary, they may be able to give some guidance on how to access a particular organ.

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Anaesthesia Anaesthesia differs from immobilization (p. 70), in that it excludes the sensation of pain, which immobilization does not do. For any surgical procedure it is necessary to employ a local or general anaesthetic, possibly in addition to immobilization. Drugs and dosages used in the anaesthesia of crocodilians have been reviewed by Loveridge (1979) and Bennett (1991). Hypothermia Lowering the body temperature by packing the animal in ice, or even placing it in a freezer, reduces its ability to react and immobilizes the animal, but does not reduce its capability to perceive pain (Kennedy and Brockman, 1965; Hartman, 1976; Ensley et al., 1979). The procedure is very stressful, and may lead to post-recovery complications. It should, therefore, never be used, even in conjunction with local anaesthesia (Bonath, 1979; Nichols, 1986; Bennett, 1991). Inhalation anaesthesia Crocodiles, like all amphibious animals, can hold their breath for prolonged periods. This may make it difcult to induce inhalation anaesthesia (Jones, 1977). However, this may be overcome by removing the tape covering the eyes, which was found to stimulate respiration in a 2.2 m Crocodylus palustris (Russo, 1979). For the induction of anaesthesia, the animals head was placed in a clear plastic bag lled with a halothaneoxygen mixture from a vaporizer, operated at a 5.5% halothane concentration with a ow rate of 5 l min 1. After 20 min the animal was thought to be sufciently anaesthetized, the plastic bag was removed and its jaws were held open by the insertion of a wooden block. However, the animal started to react, so the plastic bag was replaced for another 15 min. After that, a cuffed endotracheal tube was inserted and connected to the anaesthetic machine, which was then operated at 2.5% halothane with 2 l min 1 oxygen. After termination of the anaesthesia it took the animal 10 min to recover fully and walk back to

its pool (Russo, 1979). Apparently, the loss of the skin reex is a better indicator of the depth of anaesthesia than the loss of other reexes. This reex is provoked by applying rm pressure with a key, in a linear stroke along the side of the crocodile (Russo, 1979). In juvenile American alligators of 770 g body mass, anaesthesia was induced by 5% halothane and 95% oxygen and maintained with 3% halothane and 95% oxygen (Branco and Wood, 1993). In American alligators, Calderwood (1971) induced anaesthesia with 3% halothane in oxygen via a mask, which after intubation was continued with 1.5% halothane. General anaesthesia by injection A number of general anaesthetics have been used in crocodiles, including barbiturates, ketamine, phencyclidine and tricaine methane sulphonate. Their dosages are summarized in Tables 2.142.16. As most of these drugs are injected either im or ip, their resorption may take a long time. Recovery from this type of general anaesthesia may also be prolonged and barbiturate anaesthesia should be avoided, since recovery is especially protracted (Nichols, 1986). Local anaesthesia Local anaesthetics work best when used together with chemical restraint (see p. 70). In very small hatchlings there may be a danger of overdosing, as is the case in small birds. Lignocaine and procaine have been used for laparotomies in C. johnsoni and Crocodylus niloticus, respectively (Limpus, 1984; Kofron and Trembath, 1987) (see also below), and procaine, together with thiopental, in American alligators (Greeneld and Morrow, 1961). Xylocaine was used in conjunction with hypothermia in an American alligator, for the removal of bro-granulomatous masses (Ensley et al., 1979) (see also p. 95).

Laparoscopy Limpus (1984) examined the ovaries of 23 mature Johnstons crocodiles by laparoscopy

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93

Table 2.14. The use of barbiturates for general anaesthesia in crocodiles. Species Pentabarb Alligator mississippiensis A. mississippiensis A. mississippiensis 3.35 Length (m) Mass (kg) Dose (mg kg 1) Route References

<2.3 90180 135

A. mississippiensis A. mississippiensis Caiman crocodilus C. crocodilus A. mississippiensis Thiopental A. mississippiensis


a b

11.14 11.2

4.15.9 730

>43 1114.5 11 14.8 14.8 3.7 9 7.88.9 15.5 8.9 2030 15

By mouth By mouth ipa;b By mouth ip ipa;b ip im imc imd ip ipe

s s s

1 1

s s s u u s s

1 2 3 4 4 6 5

+ Tubocurarine ip. + Postsurgically pentamethylene tetrazole half-hourly or hourly. c Split and given in three consecutive amounts. d During induced hyperthermia 35.6C. e + Local anaesthesia with procaine. s, Satisfactory. u, Unsatisfactory. 1, Pleuger (1950); 2, Jones (1977); 3, Brisbin (1966); 4, Klide and Klein (1973); 5, Greeneld and Morrow (1961); 6, Xu et al. (1997). Table 2.15. The use of ketamine for general anaesthesia in crocodiles. Species Aligator mississippiensis Crocodylus niloticus A. mississippiensis C. niloticus Length (m) Mass (kg) 2.53 0.07 0.8100 Dose (mg kg 1) 125150 59 40100 2244 Route im im Comment h d h, s s, r References 1 2 3 4

0.652.92

h, Fine for handling only. d, Dead after 1 h. s, Satisfactory. r, Respiratory depression. 1, Jones (1977); 2, Cooper (1974); 3, Terpin and Dobson (1978); 4, Thurman (1990).

in the eld. Each crocodile was strapped to a board to prevent movement. The abdominal cavity was tightly inated with air from a compressed air cylinder, as used for underwater diving, delivered via a Veress pneumoperitoneum needle (10 cm) with a spring-loaded blunt stylet. This was inserted through the ventral body wall, two scale rows to the right of the midline and anterior to the pubic bone. A 7 mm OE trocar and

cannula with valve was inserted through the same incision, to provide an entry for the laparoscope, a Storz 26031B Hopkins telescope (OD 6.5 mm, forward-oblique viewing, 30E wide angle, incorporating bre optics light transmission) connected to a Storz 482B cold light source. The following internal structures were seen and identied during laparoscopy: intestinal loops, hard-shelled eggs in the

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Table 2.16. Other agents used for general anaesthesia in crocodiles. Agent MS222 Species Alligator mississippiensis Caiman crocodilus A. mississippiensis A. mississippiensis A. mississippiensis Crocodylus spp. C. crocodilus A. mississippiensis Mass (kg) Dose (mg kg 1) 8899 66110 1122 150 0.74 0.25 0.30.5 0.55 120 Route im im im iv iv im im Comment References s, l u h, l s u s s s ss 1 2 1 3 4 4 5 6 6

Sernylan Viadryl Saffan M99

1.44.3 Immature 10 0.112 1.56.7

MS222, Tricaine methanosulphonate; Sernylan, phenylcyclidine; Viadryl, hydroxidione; Saffan, alphaxolone/alphadolone; M99, etorphine; s, satisfactory; l, long recovery; u, unsatisfactory; h, ne for handling only; ss, satisfactory in small individuals only. 1, Brisbin (1966); 2, Klide and Klein (1973); 3, Campos (1964); 4, Calderwood and Jacobson (1979); 5, Jones (1977); 6, Wallach and Hoessle (1970).

oviducts (vaginae), soft-shelled eggs in the oviducts (uteri) and the ovaries with small or large follicles.

Laparotomy Limpus (1984) performed laparotomies on ve adult Johnstons crocodiles to examine their ovaries. The manually restrained animals were held in dorsal recumbency, the skin around the site of the incision was scrubbed and disinfected, and the incision site was injected subcutaneously with a local anaesthetic (see also p. 92). The incisions were closed with surgical catgut, and coated with a sterile spray-on wound dressing. The crocodiles were kept dry and cool for 24 h after the surgery and then returned to the water. Kofron and Trembath (1987) describe laparotomies on adult female Nile crocodiles for the examination of their ovaries. The animals were restrained manually, their legs were tied together over their backs and their eyes were taped closed. Two animals were operated on in dorsal, and two in ventral recumbency, and it was found that the latter struggled less. For the animals in ventral recumbency, the abdomen was lifted somewhat on the side of the incision by placing a

block of wood underneath. The skin was scrubbed, disinfected and a local anaesthetic was injected at several points along the line of the intended incision, transversally between two rows of scales, halfway between the last rib and the leg (see also p. 92). The skin was incised 10 cm and the different muscle layers each dissected bluntly. After the operation the peritoneum, the muscle layers and the fat layer were closed with continuous catgut sutures. The skin was closed with stainless-steel or nylon sutures. The incision was then sprayed with a plastic skin sealer containing neomycin and bacitracin, and each animal was given chloramphenicol by im injection into the base of the tail. The animals were released into the water 30 min after completion of the operation and were recaptured 13 months later, when the skin sutures were removed.

Clinical surgery Gastrotomy Pleuger (1950) describes the gastrotomy of an adult zoo crocodile (species not indicated) that had been observed swallowing a Coca Cola bottle. The animal was anaes-

Examination of Crocodiles and Clinical Procedures

95

thetized with pentobarbitol (see p. 92). The abdominal skin was scrubbed, disinfected and a longitudinal 25 cm incision was made in the midline, between two rows of scales. The skin was held back by retractors, and the abdominal muscle was incised down to the peritoneum and also held back by retractors. The stomach itself was palpated and brought to the surface through a peritoneal incision. Then a 7.5 cm incision, made through the stomach wall along the line of its greatest curvature, exposed the neck of the Coca Cola bottle. This bottle, unbroken, was removed from the stomach, together with the major portions of ve broken bottles, 39 stones, three marbles, two rearm shells, a plastic whistle and a porcelain elephant. The stomach mucosa was thoroughly sponged and the gastric incision was closed with surgical silk No. 0, which was also used to close the abdominal muscle and the subscutal skin. The skin was closed with No. 1 sutures, painted with collodion and covered with gauze sponges. The entire abdomen was then wrapped in a heavy muslin bandage. The crocodile was not allowed back into its pool for 3 weeks, after which the bandage was removed and the wound was found to have healed completely. Pleugers (1950) speculation about storage of swallowed matter in the lower oesophagus is wide off the mark: the stomach takes all the swallowed matter and the oesophagus does not act as a crop, as in fowls, or a proventriculus, as in the ostrich. While gastroliths are commonly found in crocodiles and their presence is regarded as normal, it is possible that the swallowing of large numbers of foreign bodies might be due to deranged, or stress, behaviour (see p. 290), similar to that commonly observed in ostriches (Huchzermeyer, 1998a). Whether the operation described above was in fact necessary is a debatable point; it may be the case that the bottles would have been either regurgitated or ground down. Regurgitation of hair balls and foreign objects has been observed in American alligators (Chabreck, 1996; Chabreck et al., 1996) (see p. 37). The bandage appears to have been entirely unnecessary, and the animal should have been returned to the water much earlier,

probably within 3 or 4 days, to avoid unnecessary dehydration (see p. 283). Oral surgery Russo (1979) reports on the removal of a granulomatous polyp from the palatal fold in the pharynx of a 55 kg, 2.2 m C. palustris, at the New York Zoological Park. The animal was restrained manually and anaesthetized with halothane (see p. 92), while the mouth was held open by a wooden block inserted on one side, between the jaws. The polyp measured 5 3 1.5 cm and was easily excised from the underlying tissue. Two small vessels entering the growth were ligated and the incision was closed with simple interrupted sutures of polyglycolic acid (Dexon, American Cyanamid). Ten minutes after completion of surgery, the animal walked back into its pool. It resumed feeding on schedule and the surgical site healed without complication or recurrence. An open multiple fracture of the mandible of a 1.05 m long American crocodile was operated on under general and local anaesthesia (ketamine 50 mg kg 1 and lidocaine 1%). A 1 cm piece of bone was taken out. The two ends of the fractured jaw bone were united with the help of a stainless-steel plate, stitched in place with surgical stainless-steel wire. During recovery, the lower jaw deviated towards the injured side by approximately 5 (RubioDelgado, 2000). Limb surgery Ensley et al. (1979) describe the removal of granulomatous masses from both forelimbs, plantar in the metacarpal area of a 128 kg American alligator, at San Diego Zoo. The animal was restrained physically and by hypothermia, and was given a local anaesthetic at the base of the growths. A circumferential incision was made at the base of each mass, the edge of this incision was undermined and dense brous connective tissue was excised from the centre of the surgical wound to facilitate its closure. Simple, interrupted sutures of 0.4 mm stainless-steel wire were used to close the skin. A gauze

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dressing, covered by elastic adhesive tape (Elastakon, Johnson & Johnson), was applied to each carpus, leaving the digits exposed. The operation lasted 2 h, and minimal bleeding was encountered. After the operation, the animal was housed for 6 weeks in a shaded enclosure on concrete. Dressings were changed each week and wound drainage was minimal. When the animal was returned to an aquatic exhibit, the stainless-steel sutures, with a small amount of adjacent tissue, were sloughing while being replaced by regenerating skin (Ensley et al., 1979). Yolk-sac excision The surgical removal of retained yolk-sacs has been described by Youngprapakorn and Junprasert (1994). For details, see Chapter 4 (p. 144).

Experimental surgery Gastric cannulation Sixteen C. crocodilus ranging from 30.5 to 96 cm total length were used in the experiments by Diefenbach (1975b). As repeated cannulation of the stomach, through the mouth, for the sampling of uids was found to be too traumatic, a polyethylene tube was inserted via the mouth into the lumen of the stomach. The cranial end was then led outside through an incision in the oor of the pharynx, lateral to the basihyal cartilaginous plate of the larynx. The outside of the catheter was stoppered and strapped to the animals neck with surgical adhesive tape, which resisted immersion in water. Details of anaesthesia, if any, and suture were not given (Diefenbach, 1975b). Bile stula Xu et al. (1997) implanted bile stulas into seven juvenile American alligators, between 104 and 114 cm long and weighing 4.15.9 kg, for the study of bile salts. The animals were anaesthetized by the ip injection of pentobarbital, 2030 mg kg 1 live mass,

and deep anaesthesia followed within 12 h. The animals were taped to an operating table prior to surgery. A midline incision of about 8 cm was made just caudally of the rib cage. The gall bladder was mobilized from the mesoduodenum and the cystic duct, dissected and ligated. Cholecystotomy was performed by inserting silicone tubing into the gall bladder and xing it with a purse-string suture. The tubing was exteriorized through a dorsal subcutaneous channel to an area near the hind legs of the animal, xed in position with tape and inserted into a sterile, plastic sampling bag, which was also secured with tape. After three animals had been stulated in this manner, the method was modied when it was found that the left hepatic duct in most alligators had a direct connection with the duodenum. After ligation of the cystic duct, the left hepatic duct was dissected in the mesoduodenum, double-ligated and cut between the ligations. Then the procedure for cholecystotomy and externalization of the bile drainage tubing was followed as before. The alligators were maintained in dry tanks for 57 days postoperatively and then placed in environmental chambers (Xu et al., 1997). Open-heart surgery Heart operations were carried out on 11 American alligators (1.11.5 m) by Kennedy and Brockman (1965). After immobilization by hypothermia (see p. 92), and scrubbing and disinfection of the site of incision, a midline cut between the scales was made from the distal end of the sternum, extending caudally for about 6 cm. Beneath the scales the thin, brous tissue and the muscle layer were exposed and incised to permit entry into the pericardium, which was lifted with forceps and incised longitudinally. The pericardial incision was large enough to permit delivery of the heart beyond the ventral abdominal wall. The gubernaculum cordis was clamped, cut and tied on the side of the pericardium. Near the apex of the heart, the clamp was left on the gubernaculum cordis and used for traction when manipulating the heart. After delivery of the heart, a cardiac

Examination of Crocodiles and Clinical Procedures

97

tourniquet, consisting of a heavy cotton string looped within a glass tube, was applied so as to encircle all the vessels near the base of the heart. Once the cardiac tourniquet was tightened, a time was set to measure the time of cardiac occlusion. The mean occlusion time for nine alligators was 22.5 min (range 1630 min). The ventriculotomy began just caudal to the junction of the right ventricle, with the conus arteriosus longitudinally for about 1.5 cm, and avoided major coronary vessels. After completion of the experiments, the right ventriculotomy wound was closed in two layers with a continuous suture through the myocardium and through the epicardium. Shortly before closure, the ventricle was ooded with Ringers solution to reduce the risk of air embolism. The cardiac tourniquet was released immediately after the ventricle had been closed. The heart was observed through several beats to demonstrate adequate closure and, when necessary, one or two additional sutures were applied. Clotted blood was removed from the pericardial cavity and the cavity was closed loosely with interrupted ne silk sutures to allow

drainage. The brous and muscle tissue cut during the initial midline incision was closed with an interrupted suture of No. 30 stainless-steel wire. Eastman 910 Monomer or collodion was applied to the sutured wound to strengthen and seal it. After the operation the alligator was left in a dry cage for up to 2 weeks to ensure that no infection or other problem had occurred. Five of the operated alligators died with a mean survival time of 35 days. All of them had an acute pericarditis, which the authors believed to have been due to insufcient closure of the skin wound. Sutures did rupture during violent movements of the alligators when they were caught for inspection of the wounds. Even sutures that remained intact caused local peripheral erosion around the suture of scales and subjacent tissue, with eventual disruption of the wound (Kennedy and Brockman, 1965). Another more likely reason for the high incidence of pericarditis after the operation may be stress septicaemia (p. 228) brought about by the lack of anaesthesia during hypothermia, by the hypothermia itself, by water deprivation or by the stress of frequent handling (p. 278).

Chapter 3
Important Aspects of Crocodile Farming

The contents of this chapter are not intended to be a denitive guide to crocodile farming. However, most crocodile diseases are somehow related to, or caused by, management factors, and this cannot be made clear in the discussion of the diseases unless the principles of crocodile farming have been spelled out somewhere. As there is, at present, no textbook on this subject, it became necessary to collect and present the relevant facts in this book.

Nutrition
In the wild The study of the nutrition of crocodiles in the wild is based mainly on the analysis of their stomach contents and only secondarily on the observation of their behaviour. Indigestible items, such as shells and sh scales, tend to accumulate in the stomach and may skew the results of such analyses. It is also logical to assume that prey size increases as the crocodile grows. The fact that shes are the only known intermediate hosts of the internal parasites of crocodiles further indicates the important role of sh in the diet of all crocodilians. Hatchlings start feeding on small aquatic invertebrates such as insects, crustaceans and
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snails, and later include tadpoles, small frogs and sh in their diet. As they grow, the proportion of sh increases and later birds and small mammals are also taken. Hippel (1946) examined 587 stomach contents of Nile crocodiles in Uganda, of which 141 were found to be empty apart from stones. Of the remaining stomachs, 73.1% contained sh, 14.8% amphibians and reptiles, including crocodile remains and crocodile eggs, 8.5% birds, 1.6% mammals, 0.7% insects and 36.3% plant material, the latter probably ingested accidentally. Stomach contents of Crocodylus porosus up to 180 cm in length consisted mainly of crustaceans and insects, with an increasing proportion of vertebrates (sh, reptiles, birds and small mammals) in animals longer than 120 cm (Taylor, 1979). Stomach contents of adult wild-caught dwarf crocodiles Osteolaemus tetraspis surveyed at markets in the Congo Republic comprised remains of beetles and other insects as well as spiders, scorpions and millipedes, also remains of shes, frogs, lizards, snakes, birds and small mammals (Riley and Huchzermeyer, 2000).

Energy The metabolic rate is the rate at which energy is burned. In crocodiles, as in other

CAB International 2003. Crocodiles: Biology, Husbandry and Diseases (F.W. Huchzermeyer)

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reptiles, this is dependent on the body and environmental temperature and on the energy demands of certain activities. Thus it increases sharply during the digestion of a meal (Gatten, 1980). In American alligators it was found that acetate (from fat) was preferred to glucose as a source of energy, but the major pathways of energy utilization were the same as in mammals (Black et al., 1963). Lawrence and Loveridge (1988) demonstrated that a meat diet (ox heart plus bone meal) did not full the energy requirements of juvenile Nile crocodiles. The addition of raw maize (corn) our as an energy source to the rations of spectacled caimans reduced their performance (Avendao et al., 1992), as crocodiles cannot digest raw starch. The supplementation of rations of American alligators with precooked (extruded) starch improved not only the growth performance of the alligators but also the digestibility of protein (Staton et al., 1990a,b, 1992). The same authors found a similar improvement by supplementing the rations with fat. However, fat supplementation alone of C. porosus diets did not reduce the use of protein as an energy source, but led to fat deposition instead. The digestibility of long-chain saturated fatty acids was less than that of unsaturated fatty acids, and C20:5 as well as C22:6 fatty acids were found to be essential for juvenile C. porosus (Garnett, 1985, 1988).

Minerals There is no need to supply additional macrominerals if the crocodiles are fed meat with bones. In compounded rations the macrominerals are best supplied by the addition of bonemeal. Fish meal is a good source of many microminerals (trace elements). The composition of a micromineral premix used in South Africa (Feedmix, Johannesburg) is shown in Table 3.1. The quantities given are for inclusion into 1 t (1000 kg) of dry mixed ration. In a meat- or sh-based wet ration, only one-quarter of the amount should be used, because of the water content of the ration (see also Table 3.4). A trace mineral premix used in feeding trials with juvenile American alligators is shown in Table 3.2.

Vitamins There are hardly any experimental data concerning the vitamin requirements of
Table 3.1. Mineral premix used for crocodiles in South Africa (Feedmix, Johannesburg), quantities per 1 t of complete ration. Availa-Zn Availa-Cu Availa-Mn Availa-Fe Choline Iron Copper Zinc Cobalt Manganese Iodine Selenium Chromium 40,000 mg 5,000 mg 40,000 mg 20,000 mg 600,000 mg 40,000 mg 7,000 mg 70,000 mg 500 mg 60,000 mg 1,500 mg 200 mg 200 mg

Protein While protein may be used partially as a source of energy, its main purpose in nutrition is to provide amino acids that are used in the synthesis of the bodys own proteins for the growth of body tissues. As predators, crocodiles in nature consume animal protein almost exclusively. However, in feed trials with American alligators, they have been shown to utilize isolated soybean protein equally well when it was incorporated as 40% of the total protein content of the ration (Staton et al., 1992). Total digestible protein comprising 42.548.7% of the rations gave the best performance (Staton et al., 1990b).

Availa, mineral in a metabolically available form. Table 3.2. Micromineral premix used in feeding trials with American alligators, inclusion per 1 kg of wet ration (Staton et al., 1992). Manganese Zinc Iron Copper Iodine Selenium (sodium selenite) 240 mg 200 mg 120 mg 20 mg 4.2 mg 0.1 mg

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crocodiles. Most of the recommendations are based on extrapolation from other species. A crocodile vitamin premix used in South Africa (Feedmix, Johannesburg) is shown in Table 3.3. The quantities given are for 1 t (1000 kg) of dry mixed ration. In a meat- or sh-based wet ration only one-quarter of the amount should be used. The composition of the vitamin supplement used by Cardeilhac et al. (1991) in breeding trials with American alligators is shown in Table 3.4 and the one used in feeding trials with juvenile American alligators by Staton et al. (1992) in Table 3.5.

Table 3.4. Vitamin and micromineral supplements used in breeding trials with American alligators; rate of inclusion not stated, probably per kg wet ration (Cardeilhac et al., 1991). Vitamin A Vitamin D3 Vitamin C Vitamin E Menadione Riboavin Niacin Pantothenic acid Folic acid Vitamin B12 Biotin Pyridoxine Thiamin Copper Manganese Iron Selenium Iodine 220,000 IU 55,000 IU 300 mg 14,500 IU 300 mg 132 mg 700 mg 220 mg 18 mg 0.22 mg 3.5 mg 88 mg 44 mg 18 mg 1,320 mg 176 mg 6 mg 18 mg

Home-mixed rations Home-mixed rations are often based on farm mortalities dead horses, cows, pigs or poultry. Meat from large animals usually is separated from the bones before mincing and thereby becomes decient in macrominerals (see above), whereas poultry carcasses are minced usually with the bones. However, the bones in broiler carcasses may be decient in calcium and phosphorus, as these birds are fed minimal mineral levels. Pig carcasses may provide excessive amounts of fat. The polyunsaturated fatty acids in sh oil may have become rancid if the sh is not entirely fresh when fed, and this can poison the
Table 3.3. Vitamin premix for crocodiles used in South Africa (Feedmix, Johannesburg), quantities per 1 t of complete ration. Vitamin A Vitamin D3 Vitamin E Vitamin K3 Folic acid Niacin Pantothenic acid Vitamin B1 Vitamin B2 Vitamin B6 Vitamin B12 Biotin H2 Vitamin C Antioxidant Zinc bacitracina
a

Table 3.5. Vitamin supplement used in feeding trials with juvenile American alligators, inclusion per 1 kg of wet ration (Staton et al., 1992). Vitamin A, all-trans-retinyl acetate 18,000 IU Vitamin D, cholecalciferol 2,000 IU Vitamin E, all-rac- -tocopheryl acetate 150 IU Menadione sodium bisulphite 25 mg Thiamin 15 mg Riboavin 15 mg Pyridoxine 25 mg Vitamin B12 0.042 mg Niacin 200 mg Calcium pantothenate 50 mg Folic acid 4 mg Biotin 1 mg Choline 1,500 mg Inositol 50 mg p-Amino-benzoic acid 50 mg Vitamin C 450 mg

12,000,000 IU 2,000,000 IU 120,000 mg 15,000 mg 3,000 mg 100,000 mg 50,000 mg 15,000 mg 20,000 mg 15,000 mg 30 mg 1,000 mg 1,000,000 mg 3,500 mg 80,000 mg

Not a vitamin, but added as a growth promotor.

crocodiles, causing steatitis and fat necrosis (see p. 219). Mince that is kept frozen, and thawed out and refrozen repeatedly, becomes depleted of biotin, with the resulting deciency causing nervous symptoms (see p. 217). All farm mortalities, and even other fresh meats, may contain large numbers of bacteria, including pathogenic ones. These can be

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eliminated by heating the mince, which is then allowed to cool down before vitamin and mineral premixes are added and the mix is minced a second time (Huchzermeyer, 1991a). The resulting food is a loose crumble, which does not compact on the oor of the pen as easily as fresh mince and therefore can be consumed much better by the crocodiles. Carbohydrate can be added to such a cooked ration easily by cooking a stiff maize (corn) porridge (polenta) which is added in approximately equal proportion to the cooked mince and the other ingredients (see above) before mincing the ration a second time.

Inuence of temperature on nutrient utilization In Caiman crocodilus the amplitude and frequency of gastric contractions increases with temperature, while complete emptying of a full stomach takes an average of 315 h at 15C and 99 h at 30C (Diefenbach, 1975b) (see also p. 36). In the same species, peptic activity in the stomach also increases with temperature between 15C and 35C (Diefenbach, 1975a). While American alligators kept at 32C had greater feed intake and body mass gains, their feed efciency ratio was poorer than that of alligators kept at 28C. However, the digestibility of protein appeared not to be affected by temperature (Staton et al., 1992). At 25C the digestion of lean meat by juvenile American alligators was found to be incomplete (Coulson and Coulson, 1986).

Pellets Provided the crocodiles are kept under controlled thermal conditions, within a narrow range of their preferred temperature, and are protected from disturbances and other stress (see p. 277), they will accept dry pellets as food and can be fed pellets exclusively from hatch to slaughter. Dry pellets have the advantage that they are very hygienic and can be picked up easily from the oor by the crocodiles, thereby minimizing wastage. In South Africa several crocodile farmers prepare their own pellets in different sizes depending on the size of the young crocodiles. Other crocodile farmers have turned to commercial trout pellets, also with acceptable results. In the formulation of such pellets one should probably be guided by the results of Staton et al. (1990b), although these authors were feeding their rations in the form of a thick paste, which led to serious wastage problems. Their best results were obtained at levels of 42.548.7% digestible protein and 43674421 kcal kg 1 digestible energy, with the inclusion of 6.318.8% precooked (extruded) maize (corn) and 15.827.4% fat. Note that the inclusion of such amounts of fat into dry pellets would create serious technical problems. The same authors gave 8.210.9 : 1 kcal g 1 protein as an optimal digestible energy to crude protein ratio.

Effect of nutrients on reproductive performance Cardeilhac et al. (1991) studied the inuence of various nutrients on the reproductive performance of American alligators. They divided reproductive performance into nest rate, clutch size, per cent banding and embryo survival, and analysed the effects of protein, fat, highly unsaturated fat, vitamins (see Table 3.5) and a growth promoter (Gatorcillin containing 200 mg virginiamycin and 800 mg oxytetracycline). Nest rate was inuenced by protein consumption, followed by total feed intake and highly unsaturated fat, and slightly by vitamin and antibiotic supplementation. Clutch size was affected by total fat in the diet, followed by protein and total feed. Percent banding was strongly correlated with vitamins and antibiotics, followed by highly unsaturated fat, while total fat consumption had a negative effect. Embryo survival was strongly affected by the mothers age, and the effect of nutrients was estimated to be in the following order: total fat, vitamins, antibiotics, highly unsaturated fat, protein, total feed.

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A high incidence of shell defects was caused by low calcium levels in the ration of the breeding females. The addition of extra calcium in subsequent seasons eliminated the incidence of these defects almost completely (Hibberd, 1996) (see p. 139). Note that the long-term use of antibiotics in the feed leads to bacterial resistance, and should therefore be avoided (see p. 91). It may also leave antibiotic residues in the meat, which may then not be allowed to be exported to certain countries (see p. 130).

84 mg kg 1 and oxytetracycline 300 mg kg 1 of the ration. The South African crocodile premix contains 80 mg zinc bacitracin per kg of nal ration (see Table 3.3). Note that there is growing concern about the stimulation of bacterial resistance due to the widespread use of antibiotics in animal feeds (see p. 91). Importing countries increasingly demand meats and meat products to be free of growth stimulant, hormone and antibiotic residues.

Incubation of Crocodile Eggs


Growth stimulants Nesting behaviour and physiology Various growth stimulants have been tried in the different species of crocodiles. The anabolic steroid Laurobolin was given at a dose of 1 mg kg 1 of live mass to poorly performing Morelets crocodiles by intramuscular (im) injection. The effect lasted for approximately 21 days and there was a marked improvement in growth and mass gains (Leon Ojeda et al., 1998). Similar results were obtained in Caiman crocodilus yacare that were injected at fortnightly intervals subcutaneously (sc) with nandrolone phenpropionate (Pelosi et al., 1944). Kanui et al. (1993) treated juvenile Nile crocodiles with weekly im injections of 0.325 mg kg 1 recombinant bovine growth hormone and found that this treatment stimulated appetite and growth. The authors recommend this treatment for poorly performing crocodiles kept under less than ideal conditions. The addition of taurine, an extract of ox heart, at 0.1% to the diet of American alligators resulted in greater fat digestibility and improved weight gains (Staton et al., 1992). However, the addition of 0.025 mg day 1 of L-thyroxine to the diet did not affect the growth of juvenile C. crocodilus (Avendao et al., 1992). Antibacterials are often used as growth stimulants. A combination of virginiamycin 200 mg and oxytetracycline 800 mg is supplied under the name of Gatorcillin (Cardeilhac et al., 1991). Avendao et al. (1992) used a combination of virginiamycin Crocodilians either lay their eggs in holes in the sand or build nest mounds into which they lay their eggs. While it has been speculated that these two forms of nesting have evolved during the evolution of the crocodilians themselves (Greer, 1970), it is also possible that they represent adaptations to particular environments. The hole nesters usually nest in sand above the ood level on river banks, while the mound nesters often inhabit swamps or plains without access to higher ground. Mounds made from plant material may produce incubation heat by bacterial action, and this may be benecial in a forest (swamp forest) environment where the nests cannot be exposed to direct sunlight. Different nesting substrates differ in their water content and in their resistance to gas diffusion. American crocodile eggs in sand nests were found to lose up to 15% of their initial mass due to evaporation during incubation, without apparent ill effects to the embryo (Lutz and Dunbar-Cooper, 1984). On the farm the nesting areas should all be on the same level to avoid competition for the higher nesting sites, and they should be separated by walls to allow the undisturbed use of adjacent nests (Fig. 3.1). The females continue guarding their nests even when the eggs have been lifted, and remain aggressive towards other females in the vicinity of the nest.

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Fig. 3.1. Nesting sites all on the same level and with separating walls in a Nile crocodile breeding pen in South Africa.

Physical parameters of the egg Crocodile eggs have an oblong ovoid shape and a hard shell. The shell consists of an outer densely calcied layer of vertically stacked calcite crystals, a honeycomb layer of horizontally stacked crystals, an organic layer containing a higher proportion of organic matrix to calcite crystals and a mammillary layer. The latter is more pronounced in the central opaque region of the shell and is attached to the shell membrane, which has numerous pores and is separated from the albumen by an amorphous limiting membrane (Ferguson, 1982) (see also p. 30). Embryonic development starts before the eggs are laid. Within 24 h after the egg has been laid, the embryo, which is oating at the top of the yolk, attaches its membranes to the top of the egg. By displacing the watery albumen towards the poles of the egg, it causes the shell to dry out somewhat, and this changes the optical properties of the shell and produces the visible opaque banding (Ferguson, 1982), the band increasing in size with the growth of the embryo (see Fig. 1.43). Consequently, a banded egg can be regarded as a fertile egg and the size of the banded area can be used to estimate the age of the embryo (Webb et al., 1987).

During incubation, the outer crystalline layer of the egg undergoes a degradation process, due to the acidic metabolic products of the nest bacteria which cause the formation of erosion craters. At the same time, calcite from the organic layer is mobilized for the calcium requirements of the growing embryo. Both the extrinsic and the intrinsic action weaken the shell, which facilitates hatching (Ferguson, 1981, 1982). However, one wonders whether this really is an evolutionary necessity, as most crocodile parents assist the hatchlings to emerge from the eggs. During the last third of incubation the oxygen uptake of Nile crocodile eggs at 32C is 8.11 ml h 1 (Aulie et al., 1989).

Egg collection and transport On farms the eggs should be collected as soon after laying as possible. This is often impossible if eggs are collected from the wild. Collection should be done early in the morning or late in the afternoon, not in the heat of the day, and care should be taken not to expose the eggs to direct sunlight, which would cause overheating and rapid death. Early in the morning the nesting

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areas are checked for signs of nightly activity to determine where eggs might have been laid. On some farms nightly egg-laying activity is recorded by an automatic video camera, which comes on every few hours during the night together with oodlights and does one circular sweep of the nesting areas. In the morning the tape is played back and the nests in which activity occurred are noted. During collection of the eggs, one person must stand guard to fend off the female, which might want to defend the nest. The sand is gently removed from the top of the nest until the uppermost eggs are exposed. The top of each egg then is marked with a cross with felt-tipped pen, crayon or pencil and each egg is transferred in its position to the transport box. Even though the embryo normally attaches itself to the uppermost point of the shell within 24 h after laying only, it is good practice to mark the position of farm-laid eggs as well, as occasionally embryonic development has already commenced before the eggs have been laid (see p. 30); it certainly has to be done with all eggs that have started banding.

The transport box is a styrofoam box of the same type as is used for incubation, with holes punched in the bottom as well as the lid (Fig. 3.2). If the eggs have to be transported over long distances, they should be cushioned by placing them on a layer of moist vermiculite. The collected eggs remain separated by clutch, one clutch per box.

The incubator room Crocodile eggs can be, and have been, incubated in boxes lled with sand or even in sand mounds. This may cause hygiene problems, particularly fungal infections. In the following, the most successful techniques used on crocodile farms will be described. The incubation complex should consist of a storage area for the egg boxes and the vermiculite, a cleaning and packing area, the incubator room itself and a hatching room. The incubator room should be of sufcient size to accommodate all the clutches and allow for future increase in production. It should be well insulated and allow the

Fig. 3.2. Nile crocodile eggs and a styrofoam box with holes punched into lid and bottom.

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required temperature and humidity to be maintained throughout the incubation period. The most even distribution of heat is achieved by under-oor heating controlled by a thermostat. Humidity of 9799% is achieved with the help of a humidier assisted by a fan. Covering the oor with water to achieve the necessary level of humidity can cause hygiene problems and should be avoided. Inside this room the egg boxes are stacked on stainless-steel racks, with passages between the racks for easy access (Fig. 3.3). Wood is prone to fungal growth under conditions of high humidity and the use of stainless steel is therefore recommended for all structures within the incubator room. Ventilation of the incubator room is usually provided through the door, which is opened from time to time when the operator enters and leaves. This is sufcient as the eggs consume very little oxygen (see

above) and as the air volume in the room is very large in relation to the total mass of eggs being incubated. When incubation facilities on a farm in South Africa were not completed in time, eggs were incubated successfully in the passage between rearing pens in a space-heated rearing house (Fig. 3.4). In the cleaning and packing area, the collected eggs are cleaned under running tapwater and dipped in a mild disinfectant solution (e.g. the South African product, F10, Health and Hygiene (Pty) Ltd), before they are packed into the incubation boxes. This area also contains the control panel monitoring the temperature and humidity in the incubator room. The hatching room should also have thermostatically controlled heating, should have a sink and tap for washing the hatchlings and some basins into which the hatchlings can be placed before they are transferred to the rearing house (see p. 107).

Incubation temperature The incubation temperature not only determines the sex of a hatchling (see p. 32), but also its preferred body temperature later in life. Consequently, crocodiles that are to be reared or kept in a cooler environment should be incubated at a lower temperature. As the metabolic rate depends on the body temperature, a higher rearing temperature will ensure faster growth and will therefore require a higher incubation temperature. The length of the incubation period also depends on the incubation temperature. All these factors have to be taken into consideration when choosing the temperature at which the incubator is to function, anywhere between 29C and 33C. In the last third of the incubation period the metabolic heat produced by the growing embryo can raise the temperature within the box, and this may have to be monitored if the incubator room is running at a high temperature.
Fig. 3.3. Egg boxes stacked on racks in an incubator room.

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Fig. 3.4. Incubation in the passage of a space-heated rearing house on a farm in South Africa. The enterprise had been moved to new premises and the incubation room had not been completed before the beginning of the laying season.

Humidity The humidity in the incubator room should be held just below saturation point, 9799%. Excessive moisture is absorbed by the eggs and leads to them swelling and bursting (see p. 139). Excessive moisture in the incubation medium also interferes with gas permeability and can lead to the suffocation of embryos at a fairly late stage, when their oxygen demand is at its highest. The vermiculite in the boxes should be soaked in water and then squeezed out, so that it just compacts but does not drip.

embryo. However, the eggs are exposed directly to uctuations of temperature and humidity.

Incubation in a medium Incubation in a medium copies the situation in nature, where the egg is buried in the nest. While sand and other materials have been used, vermiculite has been found to be superior, as it is practically sterile on delivery and is capable of holding a large amount of moisture. However, experience has taught crocodile farmers not to re-use vermiculite, as it is difcult to sterilize or disinfect after it has been used. A layer of 23 cm moistened vermiculite is spread on the bottom of the incubation box. The eggs are stacked in a pyramid on top of this layer and then more vermiculite is added until the eggs are covered by a layer 12 cm thick. In a different method, the eggs are stacked on the moistened vermiculite, but no further vermiculite is added, leaving the eggs open to inspection once the lid of the box is lifted.

Incubation on trays Incubation on trays requires a particularly well-controlled environment. In this method the eggs lie open on plastic egg trays on shelves in the incubator room. This allows easy access to the eggs and the removal of infertile (not banded) eggs, reducing the danger of rotting and contamination, and it also prevents overheating from the metabolic heat produced by the

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Hatching When the calculated hatching date approaches, the nest boxes are opened gently one by one. If the crocodiles in the eggs are ready to hatch they begin croaking, calling their mother. The boxes containing these eggs are taken to the hatching room, where the eggs are uncovered and those hatchlings that have hatched by themselves are taken out. The remaining eggs are examined and any further live hatchlings are assisted out of the shell. As they are taken from the box, the hatchlings are placed in a basin or bucket with clean warm water containing a mild disinfectant (F10, Health and Hygiene (Pty) Ltd) for a rst wash. They are then transferred to a nursery basin in which they remain for 1 or 2 days until their navels have closed completely, after which they are transferred to the rearing pens. The nursery basins should have sloping oors, allowing the hatchlings to come out of the water. They should also be partially covered to give the hatchlings the feeling of protection, as they do not realize that they are indoors and protected from predators (Fig. 3.5). These basins can be glass aquaria or plastic or metal basins. Some farms have a small nursery enclosure instead. However, from the point of view of cleaning and observation of individual hatchlings, smaller basins, one per clutch, are preferable. The water in the nursery basins should contain a mild disinfectant, such as a quaternary ammonium or F10 (Health and Hygiene (Pty) Ltd).

Hatchery hygiene Before the start of the incubation season, the incubator room is cleaned thoroughly and disinfected, and the heating and humidifying equipment is checked. The incubation boxes are washed, disinfected and left in the sun to be dried and irradiated. The supply of vermiculite is also checked. The boxes used for the collection of the eggs from the nests are kept separately. They are re-used for the same purpose but never enter the incubator room. On arrival at the packing room, the eggs are rinsed under the tap in running water and may be immersed in a mild disinfectant solution (F10, Health and Hygiene (Pty) Ltd), before they are stacked in the box. For the days clutches the vermiculite is soaked in clean water. Before placing it into the box the water is squeezed out that it no longer drips from the material held in the hand. As soon as the eggs have been packed in the box it is placed on the shelf in the incubator room. People working in the cleaning and packing room, the incubator room and the hatching room should wear clean gumboots and clean overalls. Visitors should not be allowed into the incubator room during the incubation season.

Rearing
Farming conditions are a compromise between the perceived requirements of the farmed animals and economically feasible

Fig. 3.5. Nursery basin with sloping oor and partial cover.

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solutions. Constraints are not only economic our understanding of the requirements of crocodiles is still very limited. While domesticated species have been selected and bred to adapt to certain given conditions, animals taken from the wild are much less adaptable. The closer one can cater for the actual needs of the crocodiles, the more likely it is that the farming enterprise will be successful. Hatchlings and juvenile crocodiles not only need food, water and space, they have very strict hygiene and other needs and a range of behavioural requirements. Not meeting these needs causes stress, and stress often causes disease and death (see pp. 46 and 278).

Rearing outside Outdoor rearing is practised in tropical countries, often in the proximity of wild crocodile populations. The crocodiles are kept in relatively small concrete-lined pens with equal water and land areas and partially shaded. The water is usually 1520 cm deep, and there are sloping sides to allow the

crocodiles to climb out of the water. Additional heating may be provided via hot water pipes which run submerged through the water areas of the pens (Fig. 3.6). While such a system is relatively cheap to build, it has several serious weaknesses. Although the additional heating may prevent cooling of the water during cool nights, there is no protection against overheating. When air (shade) temperatures climb above 36C, and the sun shining on to the shallow water heats it up to a similar temperature while heating the concrete oor of the pen even more the crocodiles have no way to escape overheating. Smaller crocodiles are more likely to suffer than larger ones, as their smaller mass heats up more quickly. This overheating is a very serious source of stress (see p. 278). The lack of temperature control also depresses the appetite to the point that crocodiles reared outdoors generally do not accept dry compound feeds (pellets). Hatchlings are instinctively afraid of any movement overhead, such as birds or even the shadow of a passing person. While these frequent disturbances could be prevented by the provision of hide boards, this is often not

Fig. 3.6. Partially shaded outdoor crocodile rearing pen with hot water pipes for additional heating on a farm in Zimbabwe.

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done, exposing the hatchlings to a constant succession of stressful events. On such farms the alarm calls of the hatchlings can be heard frequently, indicating the degree of stress suffered by the animals. Further problems encountered in outdoor rearing are ies and rats attracted by leftover feed, as well as escapees, as young crocodiles are very good at climbing over separating walls and fences (Fig. 3.7). If outdoor rearing is to be attempted during the colder months, some protection against excessive cold or temperature uctuations may have to be provided. Possible measures include: deeper water (>1 m), which will not cool down as rapidly as shallow water (but will be more expensive to change regularly); a sheltered area, e.g. under a plastic awning (Fig. 3.8); a few spots heated with infrared lamps, preferably under a shelter; an area of underoor heating, preferably also under a shelter. Protection against overheating can be afforded in outdoor pens only by the provision of deep water.

Rearing indoors Indoor rearing aims at reducing or preventing temperature uctuations, but this is done effectively only if the building is insulated sufciently to the same standard as a refrigerator or freezer room with a 150 mm styrofoam layer or similar insulation. This insulation will take care of overheating, while at the same time minimizing heating costs. Heating of the rearing house can be provided in several ways: heating the air space heating; heating the water by means of heating pipes; underoor heating, electrically or via hotwater pipes; infrared lamps. Space heating needs good insulation of the building. The larger such a unit, the lower the building cost per crocodile housed. Usually the heat is provided by oil burners (Fig. 3.9) which heat water circulated to the heat exchangers. The water for the crocodiles is brought in from a borehole at 20C and provides a thermogradient for the animals (see p. 44). The air in such a house is

Fig. 3.7. Potential escapees lying on top of pen walls.

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Fig. 3.8. Juvenile Nile crocodiles protected against excessive cooling by a plastic tent on a farm in South Africa.

Fig. 3.9. Oil burner on a crocodile farm in South Africa.

relatively dry, but a disadvantage may be the fact that the oor remains cooler than the air and that convection from the air to the body may be relatively inefcient, not allowing the crocodiles to reach optimal core temperatures, even if the air is heated to 35C. Underoor heating requires less insulation for the building. It should not involve

the whole oor area, and the water for the crocodiles should remain unheated as in a space-heated house. The air in such a unit remains relatively dry. The convection from the oor to the body of the crocodile is very efcient and therefore a lower temperature is required, maximally 33C. The water to be circulated through the pipes can be heated by oil, coal or heat-pump. While coal is

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cheaper than oil, its use is more labour intensive. Unfortunately the heat pump system is least efcient in winter, when it is needed most. Electrical underoor heating may be economical on small farms. Maintenance and repairing of underoor heating installations may be difcult and costly. Heating the water by circulating hot water in pipes is mainly used in outdoor rearing units. If used indoors, it can cause very steamy conditions. The circulating water is usually heated by coal (Fig. 3.10). If the house is insufciently insulated, overheating can occur in hot summer weather. Occasionally crocodiles become trapped under the pipes and drown. Infrared lamps (gas or electrical) are unsuitable for space heating, as their radiation cannot be controlled by thermostat. However, they can be used for heating areas in outdoor pens to provide warm spots in cold winter weather. Ventilation in insulated rearing houses may be provided through the doors only, but a more efcient system uses large extractor fans in the wall opposite the entrance door and these are operated once or twice a day to remove the ammonia fumes produced by the urine of the crocodiles (see p. 41). The ammonia and the humidity combined have a very corrosive action on all building materials. Low ceilings reduce the volume of air to

be heated but also limit the volume of air available to the crocodiles with regard to both the supply of oxygen and ammonia concentrations. Added advantages of a well-constructed indoor rearing unit are the absence of ies and rats and the efcient prevention of escapees. In a semi-open rearing house, lights tted over the pens attract insects during the night. These fall into the water and provide added nutrition and activity for the hatchlings (Fig. 3.11). Environmental chambers are insulated boxes, 2 m 2 m or larger, which are accessed through a lid. The sloping bottom is covered with water, allowing the crocodiles either to rest in the shallow water or to go into deeper water. The water is kept at a constant temperature, and there is no thermogradient allowing for active thermoregulation. Access to these chambers for feeding, cleaning and inspection is difcult, while their construction per unit housed is no cheaper than that of a larger insulated rearing house. High air humidity and ammonia levels are common problems.

Temperature The rearing temperature for crocodiles is dictated by their physiology. Digestion,

Fig. 3.10. Partially shaded outdoor rearing pens with the coal-burning heating unit in the background, on a farm in Zimbabwe.

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Fig. 3.11. Lamps over the pens in a semi-open rearing house in South Africa attract insects, which provide added nightly activity for the hatchlings.

metabolic rate and growth are at their best at a body temperature (core temperature) of 3233C. A temperature of 35C and above is stressful and may be fatal, while temperatures below 28C reduce the rate of digestion and assimilation, as well as the metabolic rate and growth. Any involuntary temperature change causes stress and reduces the appetite, while the provision of a thermogradient allows the crocodiles to adjust their body temperature to their own needs and comfort (voluntary temperature change) (see p. 55). For the crocodile itself, heating and cooling takes place more efciently in the water or from the oor of the pen than from the air. In outside rearing, the infrared radiation of the sun is absorbed very efciently, while the crocodiles may be able to counteract the effect of hot dry air to some extent by evaporative cooling. Ideal temperature conditions in an indoor rearing unit are achieved by keeping the air at 3335C and bringing in the water, preferably from a borehole, at 2025C. The water will warm up during the 24-h cycle before it is changed again but, cooled by evaporation, it will remain below 33C. Water is commonly heated in poorly

insulated rearing houses, where the heat from the air dissipates quickly through the ceiling. However, there is a serious danger on hot sunny days, when the air temperature inside the house rises above 35C and the heated water does not allow the crocodiles to cool down. This affects hatchlings more seriously than older juveniles, as the smaller body of the hatchlings reaches critical temperatures more rapidly.

Light Although they are nocturnal animals with excellent night vision, crocodiles cannot see in complete darkness. While they may be kept in darkness, a small, dim light source should provide some residual light in the rearing house. Where rearing takes place in the open, lights over the rearing pens will attract insects at night, which then fall into the pen and provide an additional feeding stimulus. However, sunlight also contains infrared radiation, which can cause overheating if the animals are not provided with sufcient shaded areas (Fig. 3.12) (see also p. 108).

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Fig. 3.12. Nile crocodile hatchlings competing for shade in the early days of crocodile farming.

Feeding While crocodiles, even small ones, need at least 36 h after a meal to empty their stomach, it is common practice to feed hatchlings and juveniles daily. If some of the animals have not been able to get at the feed on one day, due to the high stocking density, they should then be able to feed on the second day. On many farms no food is given over the weekend, which allows all the crocodiles to empty their stomach completely. As the crocodiles feed off the oor, the feed should be offered after the pen has been cleaned and the water has been changed. Only as much feed should be given as the crocodiles will consume within 30 min. Leftover feed only contaminates the water and encourages bacterial growth. Throwing the feed into the water increases the rate of contamination. Crocodiles can also be taught to take the pellets out of feed troughs (Fig. 3.13). Some crocodilian species, notably American alligators, reduce their feed intake in autumn if they are kept in natural daylight, even if heating is provided. This should not occur if they are kept in a closed environment with articial lighting. However, crocodiles reared outside should not be

fed during cool winter weather, when they cannot maintain their body temperature above 25C (see p. 111).

Cleaning and disinfection Crocodile faeces are rich in bacteria and fungi, which continue to multiply in the nutrient-rich, moist and warm environment of the rearing pens. Not only is it necessary to change the water every 24 h, but the contaminated surfaces must be washed as well. High-pressure hosing is more effective than using normal pressure (Fig. 3.14). The thin layer of fat, which covers all surfaces from leached-out and undigested fat, has to be removed from time to time by using a detergent. Only after the removal of this fat layer is it possible to disinfect the rearing pen effectively. Under normal circumstances it is recommended that the change of water and hosing down of the pen be carried out daily, while detergent and disinfectant are used once a week. However, during a disease outbreak disinfection should also take place every day. If there has been an excessive build-up of fat, it may be necessary to spray the deter-

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Fig. 3.13. Presenting pellets in feed troughs reduces wasting and contamination.

Fig. 3.14. High-pressure hosing removes faeces and wasted feed very efciently (photo published previously in the OIE Review (Huchzermeyer, 2002)).

gent on to the crocodiles as well, and to hose them down afterwards, and the disinfectant should also be sprayed over the crocodiles to remove excess bacteria from their skin. For this purpose a quaternary ammonium or combination disinfectant should be used, e.g. F10 (Health and Hygiene (Pty) Ltd).

Prevention of piling Frightened hatchlings and juvenile crocodiles tend to seek refuge by piling on top of each other in a corner of the pen (Fig. 3.15). This can lead to suffocation and death, but also to scratches on the belly skin, which

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might become infected and, in the end, may cause scars to remain. It also causes unnecessary stress (see p. 278). While rounding the corners of the pens may somewhat alleviate the problem, the solution lies in preventing frightening events and in providing adequate cover. Frightening events can be avoided by being quiet around the crocodiles and by avoiding any sudden and rash movements. One should also allow the crocodiles to become used to human presence, and workers should talk quietly to the

crocodiles while cleaning the pens and feeding them. A certain level of background noise, e.g. from a radio, also appears to have a quietening effect on the crocodiles. Adequate cover can be provided by hide boards which are distributed evenly in the pen (Fig. 3.16). This is of particular importance for the behavioural comfort of the hatchlings, but juveniles also make use of them, even to age of slaughter. The hide boards should be provided indoors as well as in outside pens.

Fig. 3.15. Frightened Nile crocodile hatchlings piling in their pen.

Fig. 3.16. Hide board providing cover to frightened Nile crocodile hatchlings and preventing piling.

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Handling of hatchlings All handling should be done as quietly as possible. Never chase a particular hatchling through the whole pen. It can be grabbed from a distance by using snake tongs (see also p. 59 and Fig. 2.6). Once caught, the hatchling is held in one hand around the neck and upper part of the body with thumb and forenger securing the mandibles and preventing sideways movements by the head (Fig. 3.17).

as they can inict quite severe bites. Sometimes they can be distracted by pulling them by their tail, although sometimes this will already elicit a snapping response. It is best to cover their head with a towel or sack, before trying to grab head, body and tail (see also p. 57).

Stocking density The stocking density should allow all animals free access simultaneously to the different components of the pen, land area and water, or warm and cool areas, as well as to the food. It depends also on the aggressiveness of the particular species, which may further increase with age. Ideally, a pen should be stocked with the number of hatchlings that could still be accommodated as preslaughter juveniles. However, a low stocking

Handling of yearlings and older juveniles Yearlings are caught with two hands, one hand securing the head, as with hatchlings, while the other hand holds the tail to prevent any wriggling (Fig. 3.18). Older juveniles have to be approached much more carefully,

Fig. 3.17. Holding a hatchling in one hand.

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Fig. 3.18. Holding a yearling with two hands to prevent wriggling.

density is costly because of the demand on costly space, while a high stocking density causes stress, ghting and injuries (see p. 278). While in the past authors tended to recommend small groups (Pooley, 1969), experience with Nile crocodiles, at least, has shown that there need not be a limit to group size, as long as each individual animal has the required space (Fig. 3.19). As stocking density is a function of the size of the animals, and since size is related to mass, it is probably best to relate stocking density to the average mass of the crocodiles in the pen. For masslength relationships see Tables 1.41.6 and 2.10. If p is the required pen size in m2, n the number of crocodiles in the pen and m the average mass of a crocodile in the pen, the formula p = (n m)/5 should apply. The divisor 5 may be species specic, and in this case applies to the gregarious Nile crocodile. A different divisor may have to be found for other species. Even the group with the lowest density of American alligators in the trial reported by Elsey et al. (1990a) exceeded this recommended stocking density. However, these authors showed that growth performance was inversely related to stocking density, the

lowest-density group having the fastest growth rate. Plasma corticosteroid levels indicative of chronic stress were directly related to stocking density (Elsey et al., 1990a) (see also p. 278).

Biosecurity Biosecurity aims to protect valuable farm stock against the introduction of infectious or contagious agents by erecting barriers between the animals and potential sources of infectious agents. This is common practice, particularly in the poultry industry. The pathogens include both crocodilespecic and non-specic pathogens. The crocodile-specic agents caiman and crocodile pox viruses (p. 157), adenovirus (p. 160), chlamydiae (p. 167), mycoplasmas (p. 167), coccidia (p. 183), pentastomes (p. 205), roundworms (pp. 192 and 194) and trematodes (p. 200) are carried by other (wild) crocodiles and may be present in the water of rivers and lakes inhabited by wild crocodiles. Pentastomes, roundworms and trematodes require sh as intermediate hosts. Non-specic (general) pathogens (see p. 172) are introduced either via the food, particularly with the meat from farm mortalities,

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Fig. 3.19. Large numbers of Nile crocodiles can be reared together, provided there is enough space.

carried by rats, ies and birds or via the water (surface water). Others are part of the normal intestinal ora (see p. 38). The most important task is to keep the crocodile-specic pathogens out of the farm, particularly the rearing section. To this end the following measures should be considered and, where possible, applied: only borehole, well or public water should be used, particularly in the rearing section; extreme care should be taken with the introduction of new stock, particularly if the animals have originated from the wild or from farms with previous outbreaks of disease; wide separation of breeding and rearing sections on the farm with separate staff working in each section, or at least different sets of gumboots should be worn in each section; separation of incubation and rearing facilities for eggs and hatchlings from eggs collected in the wild from those produced on the farm from own breeding stock; separation of water and drainage systems for the different groups (pens) in the rearing section; use of separate brooms for the cleaning of the different pens; and

disinfection of gumboots before entering any rearing pen. The parasitic worms are kept out by not feeding lake or river sh, or by boiling or freezing such sh before it can be used (Fig. 3.20). The impact of general pathogens can be reduced by not feeding farm mortalities, or at least by heat sterilizing (boiling) such meat before feeding. Feeding pellets is much more hygienic and therefore preferable to feeding fresh meat. The use of well, borehole or public water will also reduce the danger of environmental bacteria. However, the danger posed by intestinal microbes remains a cause of concern. Daily water change and regular cleaning and disinfection of the pens are the only ways to reduce this danger.

Breeding
Sustainable use, with the collection of eggs or hatchlings from the wild and the release back into nature of a certain percentage of the reared juveniles, is regarded as the farming method of choice from a conservation point of view. There is also a certain justication for captive breeding, particularly in countries and for species where collection of

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Fig. 3.20. Feeding freshwater lake sardines on a farm in Zimbabwe. This practice can cause severe ascaridoid infestations (see p. 192).

eggs or hatchlings from the wild for commercial purposes is not permitted. This section is based mainly on farming with Nile crocodiles in South Africa. It should be understood that different crocodile species may have different requirements, but certain principles may well apply to other crocodile species.

shows that the best results are obtained in very large enclosures with up to 500 females and the requisite number of males. The larger the available area, the easier the introduction of new individuals or groups into an established breeding group becomes. In small enclosures or single male groups, severe ghting often results from attempts to introduce a new member into the group.

Selection of group size Enclosure and nesting areas Most crocodiles are polygamous, with riverine and lake species usually being more gregarious and swamp and forest species being more territorial. This may affect the choice of size of the breeding group. Generally there are two systems: single male units and multiple male units. While the males establish a territory for their females, the females are territorial with regard to their nesting sites. Single male units avoid ghting between males, which can be a problem in multiple male units. The generally accepted sex ratio for Nile crocodiles is one male to ve or six or even ten females, but this might differ for different species. Experience in South Africa The breeding enclosure should be in a quiet area and the nesting sites, in particular, should be free of any outside disturbances. Visual barriers, in the form of islands, low walls or clumps of dense vegetation, should be provided in multiple male units, to allow the dominant males to establish their individual territories out of sight of each other (Fig. 3.21). The larger the enclosure, the less ghting is experienced. Walling off the nesting sites prevents ghting between the females. All nests should be on the same level, as those nesting sites highest above the water level are regarded as the most desirable ones (Fig. 3.21) (see also p. 54).

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Fig. 3.21. Visual barriers and walled-off nesting sites in a large breeding enclosure for Nile crocodiles in South Africa.

Fighting between females that are ready to lay can cause the oviduct to rupture, with resulting peritonitis and permanent sterility (see p. 200). Basking and shaded areas should also be provided for the thermal needs of the crocodiles.

Protection from excessive temperature variations Large crocodiles are less sensitive to temperature variations because of their large body mass. However, they are still affected adversely by excessive cold and heat. As the breeding enclosures are out in the open, the most important protection against excessive heat and cold is deep water. While some parts of the breeding ponds should be shallow to allow partially submerged basking, a large part of the breeding pond should be 23 m deep. The deep water does not cool down rapidly during a spell of cold weather nor does it heat up during prolonged hot weather. An alternative is the provision of articial burrows, which provide protection against both heat and cold. These can be provided in the form of a 60 cm high space of sufcient area to t a number of crocodiles and covered by a slab of concrete and a thick layer of

soil. However, they do present difculties from the point of view of maintenance and cleaning. Additional heating can also be provided against winter cold by infrared lamps in parts of the basking area. The crocodiles quickly learn to make use of the heating rather than going into the cold water. The provision of infrared heating is much cheaper than heating the water. All this applies to crocodile farms in tropical and subtropical climates. Crocodiles kept in colder climates need more sophisticated protection, from cold in particular. However, the general principles of thermoregulation and thermal requirements apply to crocodiles everywhere (see p. 44).

Selection of breeding stock Healthy, vigorous animals should be selected as breeding stock. Where farm-reared crocodiles are to be kept as breeders, one should select the fastest growers. Breeding groups should be composed of animals that are compatible in size and age. Wild-caught breeders are usually more territorial and more inclined to ght than farm-reared stock. Although the subspecies of the Nile crocodile have not yet been

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dened (awaiting DNA analysis), the interbreeding of crocodiles from different geographic regions of their distribution might not be a good idea, as it will render their progeny unsuitable for release back into the wild. Escapees from farms where such interbreeding is practised should also be regarded as a danger to the environment. In this light, the breeding of hybrids from two different species, e.g. C. porosus and C. siamensis, clearly is not acceptable.

multivitamin preparations can also be injected into it. Vitamin E and zinc are two substances that should be supplemented to boost reproductive performance (see p. 101).

Egg collection As soon as the eggs have been laid, the nest should be examined and the eggs be taken out. For this purpose one person armed with a wooden pole or a strong plastic pipe should chase the female away while the other person gently removes the soil from the top of the nest to expose the eggs. Even if the eggs are not banded, the top of each should be marked and the egg always be positioned in the same way it had been lying in the nest (see also p. 103). Although normally eggs are not banded by the time they are laid, some embryonic development takes place in the vagina. If laying has been delayed, for whatever reason, the embryo might just be in the process of attaching to the shell by the time the egg is lifted. Any turning at that stage will cause the death of the embryo (see p. 30). If the eggs have to be transported to the farm over long distances, they should be protected from severe vibration as well as from temperature changes, particularly overheating. In American alligators, Chabreck (1978) found that the best incubation results were achieved if the egg collection was delayed until the fourth week after lay.

Introduction of new stock Two dangers are associated with the introduction of new stock: the introduction of disease and ghting. Wild-caught crocodiles can carry crocodile-specic diseases and their introduction may in future endanger the rearing stock on the farm (see also p. 117). Fighting results when single crocodiles or groups are introduced into existing breeding groups. The larger the breeding enclosure, the less is the danger of ghting. In this context, one should also consider that the crocodiles to be introduced are already under stress from transport and translocation, and therefore are severely disadvantaged. If at all necessary, such an introduction should take place outside the breeding season. It is best done in combination with another procedure in the enclosure, such as draining the water and cleaning the pond, which will deect the attention of the dominant crocodiles from the introduced ones, at least initially.

Feeding The breeding crocodiles are fed once a week during the warm months, but not at all during cold weather (May to August in South Africa), as digestion and assimilation are inhibited by the cold. While some farmers believe that overfeeding leads to infertility, other farmers claim that this is not the case. Generally, breeding crocodiles are fed whole chickens or large chunks of meat with bones. Mineral and vitamin supplements can be applied to the surface of the meat and

Water change and cleaning Larger volumes of water out in the open and exposed to sunshine contain bacteria and algae, which to some extent break down the excreta of the crocodiles and thereby keep the water clean. A large proportion of the nitrogenous waste from the urine escapes into the air in the form of ammonia gas; however, the solids accumulate at the bottom of the pond in the form of mud. The amount of mud accumulating at the bottom can be reduced by the addition of suitable bacterial

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cultures that digest the organic constituents of the mud. The mud can be removed periodically, or even more or less continuously, by draining from the bottom together with partial relling or topping up. A sketch of such a bottom drain is shown in Fig. 3.22. The whole pond should never be drained during the breeding season, but this may become necessary once or twice a year, if bottom drainage has not been installed or has been found to be inadequate. A large breeding pond can also be divided into two parts by a shallow section in between, so that one part can be drained at a time. This will be much less stressful for the crocodiles (Figs 3.23 and 3.24).

Productivity and fertility Well-fed crocodiles in a suitable enclosure and under optimal conditions should be able to produce a clutch of fertile eggs per female

every year. However, this is rarely achieved. Unsuitable weather conditions, suboptimal nutrition and various stressing incidents and interactions affect the number of nests produced in the enclosure, as well as the percentage of fertile eggs laid. Stress seriously reduces male sex hormone levels and thus male fertility (Lance and Elsey, 1986) (see p. 276). This stress may be due to outside interference and to ghting between males, as well as to bad weather (see p. 278). The nutrition of the breeders normally receives the least attention and has been poorly researched. Where crocodile farming depends on captive breeding, but also in captive breeding programmes of highly endangered species, the critical importance of the well being of the breeders is usually greatly underestimated or even disregarded. The nutritional and behavioural requirements of the different crocodilian species may vary, but a successful breeding operation depends on meticulous attention to detail in the fullment of all these requirements.

Fig. 3.22. Sketch of a bottom drain for a breeding pond. When water is added, the overow is taken from the bottom, removing the accumulated mud.

Fig. 3.23. Schematic diagram showing the division of a large breeding pond by a shallow part or wall, allowing draining and cleaning of one part, while the crocodiles can seek refuge in the submersed part.

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Fig. 3.24. Crocodiles basking in the shallow water above the dividing wall between two parts of a large breeding pond on a farm in South Africa.

Articial insemination The only published work on articial insemination was done in American alligators, where it achieved considerable improvement over very poor results in the controls (Cardeilhac et al., 1988). It was found to be important that insemination into both oviducts took place not more than 5 days prior to ovulation. Therefore it is easier to use articial insemination in species in which all the females ovulate more or less at the same time, or within a few days of each other, as is the case with the American alligator. However, the collection of semen from killed males cannot be regarded as a viable procedure (Larsen et al., 1984). Larsen et al. (1992) reported the collection of semen from the seminal groove of live broad-nosed caiman by aspiration in a 3 ml syringe, and the evaluation of various semen extenders. It is unlikely that articial insemination will become a practical crocodile farming routine in the near future.

uniform size. Skinning is a highly skilled job and this skill is honed by continuous practice. In addition, the transport of live crocodiles to an abattoir is not possible because of the pernicious effects of pre-slaughter stress (see p. 125). For these combined reasons, the slaughter facility should be erected on the farm and the slaughter process should be spread over most of the year. Only small crocodile farms should consider sending killed crocodiles by refrigerated transport to an abattoir of a larger farm for skinning and evisceration. This latter practice is acceptable and does not affect the quality of the meat (Rickard et al., 1995). On some crocodile farms in the past the slaughtered animals were skinned, eviscerated and processed in the same room and on the same tables that were used for the cutting up of cadaver meat for feeding the crocodiles. This practice renders the crocodile meat unt for human consumption and is utterly unacceptable. In view of uctuating skin prices, the additional income derived from the meat can provide a stable base for any crocodile farm.

Slaughter
Crocodiles do not grow uniformly, and consequently all the crocodiles on a farm do not reach slaughter size at the same time, whereas it is preferable to market skins of a The slaughter facility Apart from the fact that the crocodiles are killed in the pen (see p. 124), which necessi-

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tates the location of the slaughter house on the farm, the crocodile slaughter facility should be of the same standard as slaughter houses used for other domestic species. The oor and walls should have a smooth and impermeable nish and the interior ttings should be made from stainless steel. All water used in the abattoir should be of potable quality and there should be changing rooms and ablution and toilet facilities for employees of both sexes. The workers should be provided with clean overalls, gumboots, impermeable aprons and caps. Hand washbasins and basins for the cleaning and disinfection of knives should be within easy reach. The abattoir should be divided into areas of different levels of contamination (Fig. 3.25). In the arrival area (A) the shot and bled crocodiles are hosed down. Here their skin could be cleansed by scrubbing with a chlorine-based sanitizer (Rickard et al., 1995) or F10 (Health and Hygiene, South Africa). They could also be immersed in ice water, although there is a risk of bacterial build-up in such a bath. From here the crocodiles are moved to the skinning area (B). After skinning the skins go to the skin processing area (C), where they are scraped and then salted and stored in a refrigerated skin room (D), which is used exclusively for storing the salted skins. The salted skins exit via another door to the grading and packing room (E). All the above rooms are part of the dirty area.

After skinning, the body is moved from the skinning room (B) to the evisceration area (F), which is semi-dirty. The viscera and other offal exit from here via the skinning and arrival rooms (B, A), while the eviscerated carcass is moved to the clean meat processing room (G), where the carcass is cut up into the different portions and the portions are packed and sealed, before they are frozen in the meat freezing room (H), dedicated to holding crocodile meat only. The packed and frozen meat leaves this area via a separate exit (J) without having to go through the dirty areas.

Humane killing The crocodile farming and ranching industry already has to overcome periodic bouts of adverse publicity aimed at the total protection of the species and opposed to the idea of sustainable use. This is a very strong reason to avoid any practices in the farming and slaughter of crocodiles that could be interpreted as inhumane and therefore give further ammunition to the anti-crocodilefarming lobby. Destruction of the brain by the use of a rearm or a captive bolt apparatus causes immediate loss of consciousness and therefore clearly is the most humane method of killing. The shock of the explosion also causes an immediate cessation of spinal

Fig. 3.25. Sketch plan of a crocodile abattoir: A, arrival; B, skinning; C, skin scraping; D, skin salting and store; E, skin grading and packaging; F, evisceration; G, meat processing and packaging; H, meat freezing; J, meat exit; single arrow, dirty ow; double arrow, clean ow.

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cord reexes. A crocodile killed in this way does not move or struggle after death. However, in a situation where the crocodile is handled before killing and therefore has to be held, the use of a rearm with live rounds is not practicable (Hutton, 1992) while the use of a captive bolt gun still is. Severance of the spinal cord by neck stabbing, using a sharp chisel and a heavy hammer, does not cause loss of consciousness. The brain of American alligators killed by this method remained perceptive for more than 1 h (Warwick, 1990). To overcome this problem Hutton (1992) suggests pithing the brain with a stainless steel rod immediately after neck stabbing, claiming that this could be done within 2 min. While this may be a considerable improvement over neck stabbing without pithing, the question arises whether such a delay is acceptable for a humane slaughter method. Even 2 min is quite a long time for an animal being killed by a painful method. Any handling of the crocodiles immediately prior to slaughter should be avoided in any case because of the meat hygiene consequences of pre-slaughter stress (see below). Where handling cannot be avoided, a captive bolt gun or the captive bolt device Zilka, driven by compressed air, should be used (Campos, 2000).

Clearly the most humane and efcient method is the use of a silenced small-calibre rearm (0.22 with low load) to shoot the unsuspecting crocodile in the pen at close range. The bullet destroys the brain and lodges below it, usually in the tongue, without damaging the skin of the chin. The point to aim at is the middle between the orbits and the supertemporal fossae (Fig. 3.26) (see also pp. 7 and 27). Since there is no struggle, the other crocodiles in the pen are not upset by this. The subsequent removal of the killed crocodiles and the hosing down of the blood does not upset or stress the remaining crocodiles either. In the end though, after repeated killing sessions, some crocodiles might become wary and try to hide or run away and may have to be shot from a greater distance. Where the skulls are to be cleaned and sold to tourists, and the hole in the frontal bone of the skull is regarded as undesirable, the crocodile can also be shot from behind, destroying the brain through the occiput (Fig. 3.27).

Pre-slaughter stress Acute stress increases the permeability of the intestinal blood capillaries and allows intestinal bacteria to enter the bloodstream, causing a septicaemia stress septicaemia

Fig. 3.26. The correct spot to aim at for killing a crocodile with a small-calibre rearm.

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Fig. 3.27. A shot through the occiput destroys the brain from behind.

(see p. 278). Normally the immune system of the animal takes care of the situation after blood corticosteroid levels have returned to normal. However, if the animal is slaughtered during the acute septicaemic stage, the bacteria may have been distributed throughout the body and may remain present in the meat. No effort at implementing strictest hygiene measures during slaughter and processing will prevent this pre-slaughter contamination of the meat, which contributes largely to the high incidence of salmonella isolates from crocodile meat three isolates out of six crocodile tails from one farm (Madsen, 1993), 14 out of 72 carcasses (Rickard et al., 1995). If crocodiles have to be handled at all before slaughter, this handling should be kept to the barest minimum. The corticosteroid response to acute stress is delayed by a few minutes, allowing a short and rapid handling procedure but no restraining, live transport or similar action. This is an important additional reason for the recommendation of shooting the crocodiles in the pen without prior handling (see above).

Skinning The skin is the major product of crocodile farming and therefore needs particular attention. Many factors can cause skin damage. Attention to detail is very important.

Bacterial degradation begins soon after the skin has been removed from the body. As a rst step, this danger is reduced by washing and possibly disinfecting the whole crocodile before skinning (Fig. 3.28). At the same time, this will also reduce the danger of bacterial contamination of the meat (Rickard et al., 1995). The cutting lines depend on whether hornback or belly skins are to be produced. Hornback skins are cut along the ventral midline and along the median aspect of the limbs (Fig. 3.29), while the cutting lines for belly skins are on the dorso-lateral aspect, leaving two rows of button scales on each side of the belly skin, and along the lateral aspect of the limbs. On the neck, the nuchal scales are left out and, further cranially, the cut moves along the dorsal midline to the occiput, then follows the caudal edge of the skull and mandibles and the median aspect of the mandibles to the chin (Plate 6 and Fig. 3.30). These cuts are performed on a table and the skin is ayed from the dorsal and lateral parts of the body, while the body is still lying on the table. Dorsally a web of subcutaneous muscles connects the skin with the vertebral column and ribs (see p. 8). Here the skin cannot be pulled off, but the aying knife must be used sparingly and never too close to the skin. Now the crocodile is hung up, head down, to prevent contamination of the tail meat in particular, and the skin is pulled off the ventral aspect. Then the skin is spread

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Fig. 3.28. Washing the killed crocodiles before skinning to remove most of the faecal contamination.

Fig. 3.29. A salted hornback skin on top of a pile of skins.

out on a table with the esh side up and the attached muscle and fatty tissue are removed by scraping (Fig. 3.31). As soon as possible after scraping, the skin should be salted to prevent further bacterial growth and to start the curing (dehydrating) process. For this purpose the skin is spread out, esh side up, on a slatted platform which is slightly raised off the oor. It is covered with high-quality coarse salt to about 50% of its own mass. In this process

the skins are placed on top of each other, separated by the layers of salt. The skins are left in this pile for a few days, but not too long to avoid excessive dehydration. Then the salt is shaken off and the skins are rolled individually and packed for transport. The growth of halophilic bacteria is not inhibited by the salt. If they are present, and particularly under warm conditions, they will attack the protein structures of the skin.

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and thoracic cavities are opened by an incision in the ventral midline continuing down the neck, the cloaca is cut loose from the surrounding tissue and all the viscera are pulled out in one movement. On many farms the viscera of the slaughtered crocodiles are fed to the breeding stock. This solves the problem of disposal and the viscera certainly have a high nutritional value. However, this practice is very questionable from an epidemiological point of view, as there is a distinct danger of perpetuating the presence of certain crocodilespecic infectious agents, which can be carried by apparently healthy slaughter crocodiles.

The meat After evisceration, the carcasses are cut into portions as required by the market, and the portions are vacuum packed, placed into styrofoam containers and frozen (Fig. 3.32). Crocodile meat is white and relatively rm. The meat of the legs is tougher than that of tail and body. Its avour lies between chicken, veal and sh. The meat yield depends on the size of the crocodile, with larger individuals yielding a higher percentage. While there are also sex and species differences, the overall yield of defatted and deboned body and tail meat can be expected to be in the region of 3040%, with a dressed carcass of approximately 65% of body mass (Gutirez El-Juri, 1990; Staton et al., 1990c; Cooper, 1999).

Fig. 3.30. Salted belly skin of a farmed Nile crocodile.

Some of these bacteria produce a red discoloration, referred to as red heat, while the damage caused by others only becomes apparent during the tanning process.

Evisceration After the skin has been pulled off, the carcass remains hanging head down. The abdominal

Fig. 3.31. Scraping the remaining esh off the skin.

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Fig. 3.32. Vacuum-packed portions of crocodile meat frozen in styrofoam containers and ready for shipping.

The meat is high in protein and low in cholesterol and energy. Details of its composition are shown in Table 3.6. The fat content of the carcass varies with the energy content of the nutrition and with the nutritional state of the individual crocodile. The tail contains the largest intermuscular fat deposits. For the composition of crocodile fat see Table 1.26. Bacterial contamination of the meat is believed to occur during skinning, evisceration and handling of the carcass, and decontamination of the skin before skinning is recommended to reduce bacterial counts obtained from the meat (Rickard et al., 1995).

Practically all the bacteria isolated from frozen Nile crocodile tail meat samples by Madsen (1993) (Table 3.7) commonly occur in the intestinal ora of crocodiles. It is also possible that bacteria are liberated into the blood circulation under severe pre-slaughter stress (stress septicaemia) (see pp. 228 and 278). Three out of three tail meat samples from one farm contained salmonellae (Madsen, 1993). Gamma irradiation of alligator and caiman meat at D values of 0.53 0.02 kGy and 0.37 0.01 kGy, respectively, eliminated salmonellae and Staphylococcus aureus (Thayer et al., 1997).

Table 3.6. Composition of crocodile meat, means of different cuts. Crocodylus porosus (Mitchell et al., 1995) 75.5 21.4 2.1 0.96 89.9 Alligator mississippiensis (Debyser and Zwart, 1991) 65.7 29.1 2.9 1.5 599 Crocodylus porosus, Crocodylus johnsoni (Mitchell et al., 1995) 75.9 21.1 1.9 0.95 91.1 438

Component Moisture (g 100 g 1) Protein (g 100 g 1) Fat (g 100 g 1) Ash (g 100 g 1) Cholesterol (mg 100 g 1) Energy (kJ 100 g 1)

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Table 3.7. Bacteria isolated from frozen crocodile meat, nine tails from two farms in Zimbabwe (Madsen, 1993). Genus Acinetobacter Alcaligenes Bacillus Enterobacter Flavobacterium F. Micrococcus M. M. M. M. Moraxella Pseudomonas P. Salmonella Staphylococcus S. S. S. Streptococcus S. Species wolf denitricans lentus agglomerans breve indologenes kristinae luteus nishinomiyaensis roseus sedentarius sp. acidovorans maltophila serov. capitis epidermidis hominis saprophyticus faecium equisimilis

parasite was proven to be infective to domestic pigs (Mukaratirwa and Foggin, 1999). However, the parasite is killed by freezing and only frozen crocodile meat is exported. The meat of wild harvested crocodiles may contain residues of heavy metals (p. 221) and polychlorinated hydrocarbons (p. 223), unlikely to be present in the meat of farmed or ranched crocodiles. However, the latter may accumulate antibiotic residues from farm animals, particularly pigs and poultry, fed to them (see p. 91). This potential problem is in urgent need of investigation, if crocodile meat is to maintain its image of being a high-quality product. Meat from healthy and hygienically reared and slaughtered crocodiles should be regarded as safe for human consumption.

Crocodiles in the bush meat trade in West and Central Africa Wild-caught O. tetraspis play an important role in the bush meat trade in several West and Central African countries. This is due to the ease with which they can be caught and kept alive until they arrive at the market, thereby providing a source of fresh meat. Conditions are inhumane, with the crocodiles remaining muzzled and tied up from capture to slaughter, and unhygienic as well. Stress septicaemia (see p. 228) kills some of the crocodiles before arrival at the market (Fig. 3.33), and large-scale muscular degeneration (Fig. 3.34) occurs due to the long period of restraint from capture to slaughter (Figs 1.4 and 3.35). In the Congo Republic the crocodiles are cut up, sold and eaten with the skin (Figs 3.36 and 3.37), while in other countries the skins are used for the manufacture of handbags for tourists (Brazaitis, 1987; Huchzermeyer and Agnagna, 1994; Huchzermeyer, 1998c). There is also the question of sustainability of this trade. While the swamp forests of the Congo Basin do not produce any usable timber and do not lend themselves to transformation to agriculture, the dwarf crocodiles inhabit only a narrow margin around the swamp forests (Riley and Huchzermeyer, 1999). This places severe

Human health risks The human health risks of crocodile meat have been reviewed by Huchzermeyer (1997) and Millan et al. (1997b). The rate of contamination of crocodile meat with salmonellae (p. 164) depends on housing, feed, slaughter techniques and the hygiene practices under which crocodiles are reared. While chlamydial infections (p. 167) are common on some crocodile farms in southern Africa, it is unclear whether the agent involved in these cases can infect people, and no human cases of chlamydial infection originating from crocodile meat or from contact with infected crocodiles have been reported. Mycobacteriosis (p. 170) is very rare in crocodiles, and neither Mycobacterium tuberculosis nor M. bovis are believed to be able to infect crocodiles because of the low body temperature of these reptiles (Huchzermeyer and Huchzermeyer, 2000). Tapeworm cysts (sparganosis) have been found in crocodile meat in a few instances only (see p. 203). Trichinellosis (p. 197) has been found in crocodile meat produced by several farms in Zimbabwe, and the

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Fig. 3.33. Stomach and intestine of an African dwarf crocodile which died from enteritis and stress septicaemia before slaughter.

Fig. 3.34. Muscle degeneration in an African dwarf crocodile slaughtered at a market in Brazzaville.

limits on available habitat and also makes the existing populations accessible to hunters.

medicinal uses of crocodile organs or tissues. The uses and beliefs are enumerated here uncritically and without any claim of completeness. Fat In several cultures crocodile fat is applied externally to treat skin ulcers and burns, but

Medicinal use of crocodiles and superstitions Cultural beliefs of the magic properties of crocodiles may be at the root of some of the

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Fig. 3.35. Live African dwarf crocodiles arrive at the market in Imfondo, Congo Republic.

Fig. 3.36. African dwarf crocodile about to be slaughtered at a bush meat market in the Congo Republic. Note pieces of crocodile meat with skin lying on the table.

also to treat painful joints. Internally it is taken as treatment for respiratory ailments, particularly asthma (Ross, 1992). Meat Regular consumption of crocodile (caiman) meat is said to promote the regrowth of hair in men suffering from male-pattern baldness (Wycombe, 1992). However, the abundant

hair growth seen in many South American tribes may be due more to genetic than nutritional causes. Bile and penises Dried crocodile gall bladders with the bile and dried crocodile penises are sometimes collected and bought up for the Chinese market.

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Fig. 3.37. African dwarf crocodile cut into portions for sale.

Spinal cord In the Congo Republic it is believed that the pigmented spinal cord (the black worm) must be removed from a slaughtered crocodile, because when left it renders the meat unpalatable. In fact, its removal can be witnessed routinely on markets where crocodiles are slaughtered. After having been severed close to the head it is pulled out cranially while the crocodiles back is tapped lightly with the back of the machete. A benecial side-effect of this procedure is the immediate cessation of reex movements (see also p. 80). Brain In South Africa crocodile brain is regarded as highly toxic in some rural cultures, and brain has been said to have been given to intended murder victims.

stewed, as is done in West Africa. For frying, use butter or olive oil and do not overcook. Preferably do not cook the meat in the gravy, but rather prepare the gravy separately and pour it over the meat when serving. Basically, prepare crocodile meat like any other white meat (Page, 1996).

Crocodiles in Zoos and Private Collections


While zoos generally subscribe to the principles of conservation and claim to play a role in the survival of endangered species, there are few zoos where these principles are applied to the housing and care of their crocodiles. Keeping crocodiles in zoos or private collections is subject to the same principles as keeping them on farms, with the difference that the farming of crocodiles is ruled more by strict economic considerations and less by aesthetic ones. In all cases, the welfare of the individual animal should be of prime importance. The CITES permit entrusts the animals life to the owners care. By providing a stressfree environment and by catering for all its other needs, one can ensure that the animal will stay alive for its normal life span and

A few hints for cooking crocodile meat The unique but delicate avour of crocodile meat should be complemented and enhanced but not drowned. Therefore it is important to keep recipes simple. Tail and body meat can be roasted, fried, grilled or deep fried, while the legs and some of the body parts are best

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possibly also reproduce, thereby actively contributing to the conservation of the species.

Thermal requirements While crocodiles, particularly larger specimens, apparently can tolerate prolonged exposure to low temperatures, such exposure causes considerable stress and affects the immune system as well as metabolism. Tropical crocodiles are more cold-sensitive than subtropical ones. Even in winter, the latter must be allowed to achieve a core temperature of 32C at least once a day. A natural thermogradient, consisting of sun and shade, warm shallow and cool deep water, can be provided to crocodiles that are kept outdoors. Indoors there should be a thermogradient between heated and nonheated environments. Radiation or underoor heating provides the upper end of the gradient, while cooler air and cooler water (never below 20C) constitute the lower end (see also pp. 44 and 111). Overheating is even more stressful than exposure to low temperatures. Although crocodiles are tropical or subtropical animals, they have to be able to maintain a core temperature of not more than 34C even if the air temperature in the shade goes above 40C. In nature they achieve this by making use of deep water or of burrows. To a limited extend they can also make use of evaporative cooling, particularly by gaping. Prolonged exposure to excessive heat causes the immune system to fail and encourages the establishment of bacterial and fungal infections, often of faecal origin, which lead to the death of the animal 410 weeks later (see also p. 228). It should be noted here that hatchlings and small juvenile crocodiles are more severely affected by overheating, as their small body mass heats up more quickly than that of larger crocodiles.

most of the day they are seen lying still, sleeping or trying to thermoregulate. This may lead to the mistaken view that captive crocodiles do not need much space. However, they do have a need to exercise, on land as well as in the water. Therefore the minimum length of an enclosure for a single crocodile should be equal to twice the length of the crocodile and its width equal to one length of the crocodile. An enclosure for several crocodiles should be larger, although not necessarily a multiple of the minimum for a single crocodile. For larger groups the rules of stocking density, formulated for the rearing of farm crocodiles, apply (p. 116). The species of crocodile also needs to be taken into consideration. Gregarious species, such as the Nile crocodile, tend to be tolerant of each other and can be kept in groups, while other species prefer to inhabit a territory alone or at best with one sexual partner. As a general rule, crocodile species inhabiting large rivers and lakes are more gregarious than those inhabiting forests and swamps. In all cases one should familiarize oneself with the requirements of a particular species before designing the enclosure or assigning a newly acquired animal or group to an existing exhibit. Where larger groups are kept together in one enclosure, the space should be arranged in such a way that a dominant animal cannot see or survey the whole enclosure from any one point, thus allowing other individuals to nd their own separate territories (Fig. 3.8) (see p. 119). Different species of crocodiles should never be mixed, as this may lead to stressful situations and ghting. It might also encourage hybridization, which should be strictly avoided (p. 136).

Land and water areas The available space should be divided into approximately equal proportions of land and water areas. While the land area in larger outdoor enclosures can contain natural soil and be covered by vegetation, it is necessary for indoor enclosures to be covered to a large extent by a cement oor or tiles. While

Space Crocodiles are nocturnal animals and therefore their activity is rarely witnessed, as for

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Fig. 3.38. Ample space, division of territories and pleasing aesthetics at an indoor Nile crocodile exhibit in France.

crocodiles, with the exception of gharials, walk on land, they always slide back into the water. This sliding over roughly nished concrete causes skin abrasions, particularly under the mandibles, the soles of all four feet and the belly, which easily become infected. It is therefore recommended to provide an extremely smoothly nished surface close to the water, as can be achieved with a coat of epoxy resin paint. In outside enclosures the water is needed as part of the thermogradient. It should be deep enough (>1.5 m) in parts to provide the two separate thermal environments shallow, warm and deep, cool water. Running water tends to be of even temperature and therefore is not as suitable for outdoor enclosures. Indoors the water should be deep enough in part to allow submersed swimming, >0.60 m for adult crocodiles. Another function of the water is the absorption of the excreta of the crocodiles. A large proportion of the nitrogen in the urine is excreted in the form of ammonium carbonate, which evaporates from the water and can produce an unpleasant smell in an indoor exhibit. The ventilation necessary to remove this smell may adversely affect the thermal environment, particularly where

space heating is used to provide the necessary warmth. As ammonia is heavier than air, it should be extracted close to the ground and not through the ceiling. On the other hand, the advantage of this evaporation is that less of the nitrogenous waste remains in the water. In a large volume of water and in the presence of sufcient light, algae and aquatic bacteria can deal efciently with the remaining dissolved wastes, as long as the sludge is removed regularly from the bottom (p. 121). Smaller volumes of water may have to be ltered continuously or changed regularly.

Cover Where crocodiles are exposed to direct sunlight, a shaded area is necessary for them as part of the thermogradient, just as much as a basking area. In addition, one has to consider the fact that hatchlings and juvenile crocodiles are afraid of open skies and seek some form of cover for protection when alarmed. This cover can be provided easily by ornamental plants with large leaves, which can be arranged in a way that the crocodiles under cover remain visible to the visitor,

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while feeling protected from any possible threats from above. Crocodiles have this fear of the open both indoors and outdoors (p. 114). The stress of not being able to seek cover may lead to immune failure, infections and deaths (pp. 228 and 278).

Hybridization, the interbreeding of two different species, happens quite easily in crocodiles but does not serve any purpose at all and should be avoided at all cost, as it runs against the principles of conservation. For this reason sexually mature crocodiles of different species should not be kept together in the same enclosure. Protection of visitors All crocodiles are dangerous and visitors can behave stupidly. Such behaviour is based partially on ignorance and partially on a general feeling of safety in a civilized society and environment. It is motivated by wanting to interact with the animal, which is seen lying immobile in its pen. In the city-dwellers mind actual dangers are relegated to entertainment and witnessed only on television and in videos. They do not happen in real life. A basking crocodile may appear absolutely harmless and may tempt the visitor somehow to interact with it. Visitors also like to hold up their children to give them a better view of an animal lying directly below. Rarely do they realize how fast and how high a crocodile can jump. These are possibilities that have to be taken into account in the design of a crocodile enclosure, even in private collections to which visitors have access only occasionally.

Feeding Hatchlings, and possibly juveniles as well, should be fed boiled minced meat or sh with added minerals and vitamins (see p. 99). Meat, ox heart and liver lack calcium and phosphorus, and crocodiles fed exclusively on them develop mineral shortages and bone diseases, such as osteomalacia and osteoporosis (p. 211). Feeding live food may stimulate the appetite, particularly of newly housed, disoriented hatchlings, but may be objectionable on ethical and aesthetical grounds. Small tropical sh (guppies) or cultured insects (crickets and cockroaches) are suitable as starters for hatchlings. Feeding should take place at a time of the day when the crocodiles have attained their optimal core temperature not early in the morning after a cold night. The inert feed should always be offered on land so as not to soil the water, and unused feed should be removed from the pen, after the crocodiles have all eaten.

Breeding, hybridization Where possible, breeding should be allowed or attempted, particularly in the rarer species. This entails the provision of a suitable nesting area, either with deep sand for hole nesters or with sufcient leaves or other substrate for mound nesters. While many species use sunny places for nesting, the forest species generally build their nests in the shade. In single-pair enclosures it is possible to allow natural incubation, climatic conditions permitting, and even natural rearing, while under other conditions the eggs should be removed from the nest as soon after lay as possible and incubated articially. For details of articial incubation see p. 102.

Animal Welfare
Climatic adaptability As a rule of thumb, species with a wide geographic distribution show a higher degree of adaptability than those with a very limited range. The actual conditions in their natural habitat, and particularly the components of the thermogradient within it, will dictate the conditions under which the crocodiles will thrive in captivity. Mere survival is a poor measurement of adaptation and well-being, as large crocodiles may take years to die a slow death of stress, malnutrition and incidental infections. The one point that cannot be overstated is that the thermal require-

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ments are absolutely central to the welfare of all crocodiles.

this pipe rather than any pain that could possibly be caused by such a light instrument (see p. 103).

Behavioural requirements Transport The need for crocodiles to be able to thermoregulate has been explained above (see also p. 44). Young crocodiles want to be able to seek visual shelter against any perceived threat from above (see p. 114). The requirements for space and territory vary with age and species. This not only affects group size and stocking density, but also, in breeding colonies, the provision of adequate territories and nesting sites (see p. 119). Crocodiles are stimulated to feed when they see other crocodiles feeding. In a farm situation this means that all crocodiles in a pen should be able to feed simultaneously. Weaker animals being bullied away from the feed by stronger animals may later not want to go back to the feed and eat what has been left over. Before transport, crocodiles have to be captured and restrained, either physically or chemically. The details of these actions have been discussed in Chapter 2. Transport and all handling are very stressful and therefore should be carried out as quietly, efciently and speedily as possible. The mouth should be taped shut, leaving the nostrils clear, and care should be taken that the nostrils remain clear as long as the animal is restrained. The eyes should be covered with cotton gauze swabs and also taped closed to avoid any visual disturbance of the restrained crocodile (Blake, 1993). Forcing the eyes closed also has a quietening effect on the animal and prevents unnecessary struggling. Crocodiles should always be held and transported in a belly-down position. While they are in a belly-up position the strong righting reex will induce them to strain and struggle. When moving and rolling a large crocodile, the legs should not be used as handles, as they can easily be dislocated. While being restrained, and particularly during transport, the crocodiles cannot thermoregulate. Overheating can occur when they are left exposed to the sun, and excessive cooling can occur through the wind chill factor if they are moved on an open vehicle, particularly in cold weather. If there is a danger of overheating, wetting the crocodiles may allow them to cool down by evaporation. Transport stress, like any other severe stress, reduces the resistance of the crocodiles against infections, and consequently stress septicaemia always occurs (see p. 228). If the crocodile is transported under cold conditions, e.g. in winter, and after arrival is unable to reach an optimal body temperature, it will not be able to ght off this septicaemia. This is the most common cause of post-transport mortality in larger crocodiles after transport in winter conditions.

Farming conditions On the farm it is in the owners interest to have well-nourished and stress-free crocodiles, as many disease outbreaks are triggered by stress. Well cared for crocodiles are most likely to perform to the farmers expectations. Overcrowding, handling and sorting are common causes of stress (see p. 278). Handling should be kept to a minimum and should be done as quietly as possible. Hatchlings, in particular, are afraid of being approached too closely. If they have to be caught, it is best done from a distance with a pair of snake tongs (see p. 59). Insufcient heating and overheating both are important stressors. At all times the crocodiles should be able to thermoregulate and keep their body temperature close to the preferred optimum of 3233C. During egg collection the female guarding the nest can best be driven off with a long piece of plastic piping (heavy gauge, 5 cm diameter, 3 m long). The sound of the impact scares the female away when hit with

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Transport stress also often causes the animals to stop eating. They then fall into hypoglycaemia, which further suppresses the appetite. Such crocodiles may never start eating again (see p. 282). Stress hypoglycaemia can be prevented by dosing the immobilized crocodiles with a sugar solution by stomach tube before the actual transport begins (Fig. 2.32) (personal communication, P. Watson, Maidstone, 1999). Painful procedures The ability to feel pain has an important defence function: it induces an animal to avoid pain and injuries and therefore maintain its bodily integrity. Crocodiles have small brains and therefore some of the brain functions of mammals are delegated to reex centres in the spinal cord, but this does not mean that crocodiles cannot feel pain. There is therefore no excuse for not using anaesthesia for potentially painful procedures. It should be noted that chemical immobilization has no anaesthetic effect. Under chemical restraint the animal remains fully conscious of its surroundings and fully capable of feeling pain. Details of anaesthesia have been discussed in Chapter 2. Humane slaughter Where we take it upon ourselves to keep crocodiles in captivity and to use (farm)

them for our own prot, we are under a moral obligation to do this in the most humane and enlightened way possible. Obviously, slaughter is one of the most important aspects in this context. This matter has already been dealt with in Chapter 2 and above, but some aspects need further discussion. The slaughter process potentially consists of two separate components, the capture, restraint and transport of the animal to be slaughtered and the actual killing itself. The capture, restraint, handling and transport of the animal to the slaughter plant cause intense fear and a high level of stress. The effect of the stress-induced septicaemia and its effect on meat hygiene and meat quality have been explained in detail above. From this it becomes clear that preslaughter handling should be kept to the barest minimum, if it cannot be avoided altogether. The only acceptable methods of killing are those that cause an immediate cessation of brain functions, ideally by the destruction of the brain. Shooting the unsuspecting crocodile in its pen with a small-calibre re arm into the brain is by far the best and most humane method. Where the animal has to be handled before slaughter, captive bolt or compressed air devices are the next best choices. Neck stabbing, particularly without, but also even with, subsequent pithing of the brain, is clearly inhumane and should not be used at all.

Chapter 4
Diseases of Eggs and Hatchlings

Diseases of the Egg


Without going into any detailed and elaborate denition of disease, this chapter deals with any defect, fault or infection that could cause an embryo not to develop or to die.

Shell defects The shell protects the embryo against physical damage, but during embryonic development gas and water exchange also have to take place through the shell. The porosity of the shell determines the efciency of this exchange. Wink et al. (1990) found American alligator eggs with early embryonic mortality to have a lower degree of shell porosity and the existent pores plugged with undetermined material when compared with the shells of eggs with normal embryonic development. The same authors also found farmproduced eggs to be less porous and of lower hatchability than eggs collected from the wild. Hibberd (1996) reported the following shell defects in Crocodylus porosus eggs: soft shells, partial shell formation, complete absence of the shell with only the membrane being present, additional calcareous protrusions on the external surface of the shell (pimpling), under- or oversized eggs and

eggs of deformed shape with incomplete sealing. A low level of calcium in the ration of the breeding females was believed to be the cause of these shell defects, and the supplementation of the pre-breeding ration with calcium almost eliminated their incidence in the subsequent breeding season. Eggs incubated in a very moist environment tend to absorb excessive amounts of moisture, which leads to a build-up of internal pressure and the eventual cracking of the shell, with typically multiple, parallel, longitudinal cracks of the shell, but leaving the membrane intact (Fig. 4.1).

Early embryonic deaths Early embryonic deaths in farm-bred American alligator eggs were found to be linked to, and probably caused by, low shell porosity, thought to interfere with gas exchange (Wink et al., 1990) (see also above). Early embryonic deaths can also be caused by inadvertent turning of banded eggs during collection or inspection, which dislodges the embryo from its attachment to the shell and lets it sink into the yolk sac. For the collection of eggs from the wild, Blake (1992) recommends waiting until the embryos are at least 4 weeks old (see also pp. 103 and 121).
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Fig. 4.1. Cracked shell of a crocodile egg after excessive water absorption.

Poor hatchability Poor hatchability is the result of all the causes of infertility and embryonic deaths. After excluding infertility and infectious causes, there remain incubation conditions (p. 105), the nutrition of the female crocodiles (p. 101) and possibly some genetic factors relating either to a lack of adaptation to incubation conditions or to genetic defects (lethal factors). An investigation into poor hatchability therefore has to eliminate the various factors step by step. The seasonality of crocodilian breeding can cause this process to be drawn out over several years. Crocodile farmers rarely submit unhatched eggs to a laboratory for examination. Much work remains to be done in this eld.

Infertile eggs Infertile eggs can be recognized during incubation by their failure to develop banding. However, if the embryo dies before it has attached, no banding would be visible. On many crocodile farms the eggs are collected the morning after they have been laid. They then show no banding and no care is taken about keeping the egg in the same position in which it has been found. However, there is a suspicion that the embryo becomes sensitive

to position damage during the process of attachment, before the rst sign of banding becomes visible (see pp. 30, 103 and 121). Theoretically, any egg that has been laid should have been able to be fertilized. In large multiple-female and multiple-male breeding groups, all females should have been the subjects of multiple copulations. If all females in a single-male breeding group were producing infertile eggs, this would point at male sterility. However, copulation takes place a while before ovulation. During this time the sperm survives in the oviducts. If conditions in one or both oviducts are not conducive to sperm survival, fertilization of the ovulated eggs will not take place. Such conditions can be created by bacterial infections, either ascending from the cloaca or descending from the infundibulum after a peritonitis, which could have been caused by trauma (penetrating bite wound) or stress. The ghting of females for nesting sites could be responsible for both causes of descending infections.

Bacterial infections of eggs and embryos Theoretically, bacteria can infect the egg either transovarially through an infection of the yolk, or after hatch, through the shell. The transovarial route can be used by very few bacterial species, and no cases of transo-

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varial bacterial infection of crocodile eggs have been reported so far. The shell and the membranes present a certain barrier to penetration by bacteria. This is further supported by an antibacterial action of the albumen, known in bird eggs but not yet conrmed for crocodile eggs (see p. 30). This combined action is strong enough to ward off the challenge presented by small numbers normally present in a natural incubation environment. However, slight cracks in the shell allow easy access to bacteria. Where such eggs become rotten, they can present a danger of heavy contamination for adjacent eggs in the nest, which can easily overcome the relatively weak defences of the egg. This kind of contamination is particularly important in articial incubation, where large numbers of eggs are being handled. The preventive measures are based on strict hygiene. Only clean eggs are to be set. Washing eggs under running water prevents the build-up of bacteria in the washing water. After washing, the eggs can be dipped in a disinfectant solution (quaternary ammonium or F10 (Health and Hygiene, South Africa)). Cracked eggs are to be discarded and only clean incubation medium is to be used. A nonorganic medium such as vermiculite is practically sterile when unpacked. However, one should never attempt to sterilize it for re-use (see p. 107). The sand in the nesting sites can also become contaminated over time, particularly if eggs were broken. It may therefore have to be replaced after a few years of use. Infected eggs may show small, brown, circular lesions under the shell, on or near the chorioallantois. Schumacher and Cardeilhac (1990) isolated Enterobacter cloacae, Citrobacter sp., Proteus sp. and Pseudomonas aeruginosa from these lesions, as well as fungi (see below). All of these are part of the intestinal ora and point at faecal contamination as the source of the problem (see p. 38).

challenge. Hibberd (1994) found that the pore size of C. porosus eggs was sufcient to allow hyphae and spores to pass through. She also found growth of hyphae along minute cracks. The fungi may not kill all the affected embryos during incubation. Consequently some infected hatchlings may die very much later (Hibberd and Harrower, 1993). Fungi isolated from C. porosus eggs were Fusarium solani, Paecilomyces lilacinus and Aspergillus sp. (Hibberd, 1994) and from Alligator mississippiensis eggs Fusarium oxysporum, Paeciliomyces aviotti, Penicillium fellucanum and Aspergillus niger. However, of these, only Fusarium oxysporum was found to produce lesions on the egg membrane after inoculation of disinfected infertile eggs (Schumacher and Cardeilhac, 1990). The danger of fungal infection is higher in mound-nesting crocodile species because of the plant material used in the construction of the nest mounds.

Protozoan infections of eggs and embryos Coccidia were found in tissues of dead embryos of Caiman crocodilus fuscus (Villafae et al., 1996). As certain crocodilian coccidia have a tendency to cause generalized infections, it is possible that in this case some coccidia had settled in the ovary and were transferred to the egg during ovulation (see also p. 183).

Drowning Excessive amounts of moisture added to the incubation medium interfered with gas exchange and caused 100% mortality in almost mature Nile crocodile embryos (own observations). The chorioallantois, which develops inside the shell, acts as the lungs of the embryo (see p. 30). As the embryo grows, its demand for oxygen increases. This makes the later stages of the embryo particularly vulnerable. While the incubation medium should be moist, it should not be wet. The incubation medium protects the eggs from

Fungal infections of eggs and embryos Fungi present in the nesting medium, on the shell or in the incubation medium can penetrate the shell, particularly if there is a severe

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temperature and humidity uctuations, but it should not interfere with gas exchange.

Diseases of the Yolk-sac


Diseases of the yolk-sac are part of the complex of hatchling diseases. Here they are dealt with in a separate section as they include a number of different conditions.

Yolk-sac infection The yolk-sac of the crocodilian embryo is connected to the intestine at the junction between jejunum and ileum by the vitelline duct, which remains open for the extrusion of the non-soluble fraction of the yolk, which is digested in the intestine (see p. 30). The soluble fraction of the yolk is taken up into the blood circulation via the placenta-like tissue that develops on the inner surface of the yolk-sac. A pre-hatch bacterial contamination of the egg, and the consequent infection of the embryonic membranes, can lead to a navel infection, omphalitis, when some of the infected membranes, together with the yolk-

sac, are drawn into the abdominal cavity just prior to hatch. From such a navel infection the pathogens can spread through the yolk-sac wall into the yolk. Salmonella arizona, coliforms, Pseudomonas aeruginosa and Aeromonas hydrophila, as well as fungi including Fusarium sp., were isolated from shell membranes of unhatched crocodile eggs in Zimbabwe (Foggin, 1992a). After hatch, with the rst exposure to the environment, the intestine is colonized by whatever bacteria have arrived rst. Potentially pathogenic bacteria can, under certain conditions, penetrate through the patent vitelline canal into the yolk-sac and cause its infection. As crocodile embryos develop at different speeds, but all hatch together, the navel of some of the hatchlings may not have healed completely at hatch, making it vulnerable to infection. If such a hatchling is placed into contaminated water, or on to a contaminated surface, a navel infection can result, and from there the yolksac will become infected. The infection of the yolk-sac and the yolk therein causes the vitelline canal to close (Fig. 4.2). This leads to the retention of the yolk-sac, and the affected hatchling does not get the nutritional boost provided by the yolk (Fig. 4.3). The bacterial degradation

Fig. 4.2. Nile crocodile hatchling with infected yolk-sac. Note the enlargement and the coagulated appearance of the contents due to the exudation of brin.

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(putrefaction) of the yolk further produces toxic metabolites which are resorbed from the yolk-sac. The bacteria may remain alive in the yolk-sac and at a later stage some of these bacteria may be able to leave the yolksac under certain conditions and then cause septicaemia. Omphalitis The navel being in close contact with the yolk-sac, the infection of one invariably causes the infection of the other. The two possibilities of navel infection have been discussed above. However, a direct infection of the open navel from a contaminated environment is the most common occurrence. The very large numbers of hatchlings handled on a commercial crocodile farm can lead to a rapid build-up of contamination. This calls for the strictest possible hygienic measures, disinfection of hands and implements, and the release of the hatchlings into a mild disinfectant (quaternary ammonium or F10 (Health and Hygiene, South Africa)) solution for the rst 24 h after hatch (see p. 107). In nature such a high build-up of contamination does not occur and, in addition, the hatchlings are exposed to a normal bacterial ora from the moment they are immersed into the water of their nursery, from where

normal intestinal colonization will take place immediately. There is a very delicate balance between contamination and a normal environmental ora, which cannot be reproduced under intensive farming conditions.

Yolk-sac retention Inamed yolk-sacs Retention of the yolk-sac can be caused either by low rearing temperatures or, more commonly, by infection. The mechanisms involved in yolk-sac infection have been discussed above. Infection and inammation of the vitelline canal cause it to close, preventing any further extrusion of yolk into the intestine for digestion. The inammation of the absorptive tissue in the wall of the yolksac causes the exudation of brin, which in turn causes the contents to take on a creamy or dry, cheesy, caseous, inspissated appearance (see Fig. 4.2) (Jacobson, 1984; Friedland, 1986; Foggin, 1992a). In such cases the yolksac is transformed into a typical briscess (Huchzermeyer and Cooper, 2000) (see p. 46). Continued inammation and exudation of brin may cause the yolk-sac to swell to considerable size and to rupture, with consequent spread of the infection and inammation to the peritoneal cavity (Friedland, 1986) (see p. 144).

Fig. 4.3. Older Nile crocodile hatchling with non-resorbed yolk-sac still attached to the intestine.

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Hydropic yolk-sacs The retention of hydropic yolk-sacs with watery contents has been described by Youngprapakorn and Junprasert (1994). The cause of this condition remains obscure. Symptoms of yolk-sac retention Retention of the yolk-sac deprives the hatchlings of essential nutrients needed for a good start. It also leaves a focus of infection inside the body, from which bacterial metabolites may be absorbed, leading to a toxaemia. Consequently, hatchlings with retained yolk-sacs do poorly, usually refuse to feed and become emaciated with a prominently swollen abdomen. Thermal treatment Foggin (1992a) and Youngprapakorn and Junprasert (1994) recommend keeping such hatchlings at elevated temperatures of 3234C, and to withhold food until the yolk-sac is resorbed. However, this treatment promises results only in cases where the yolk-sac has not become infected. Surgical excision Where the heat treatment is unsuccessful, Youngprapakorn and Junprasert (1994) recommend the excision of the yolk-sac with the following steps (quoted verbatim):
No anaesthesia is needed during a 1020 min operation. 1. Fix the affected hatchling on a board in the supine position. 2. Clean thorax, abdomen and proximal hind limbs with an antiseptic (Providine and ethanol 70%). 3. Make an incision from 0.5 cm cranial to the palpable mass along the abdominal midline to the pubis. 4. Cut through the peritoneum to expose the yolk sac. 5. Dissect any adhesions between the yolk sac and abdominal viscera. 6. Ligate blood vessels running from the intestine to the yolk sac and cut free the yolk sac.

7. Clean carefully if the yolk sac has ruptured and spilled its contents into the peritoneal cavity. 8. Suture peritoneum and skin in one continuous suture. 9. Clean the abdominal area.

After the operation the hatchling should be kept in a clean, dry and warm place on a sheet of cloth and observed for any postoperative bleeding. Also, check if defecation occurs, which will indicate freedom from obstructions caused by the operation. After 34 days the hatchling is allowed to swim in clean water for a while each day, after which the sutures are cleaned. Once the wound has healed completely, the hatchling can be returned to the rearing pond. The authors report a success rate of 77%.

Rupture of the yolk-sac Continued inammation of the yolk-sac with exudation of brin can cause the yolk-sac to swell to such a size that it nally ruptures (Friedland, 1986) (see also p. 143). However, the brinous contents are no longer liquid and therefore do not spill out. Consequently the peritonitis caused by the rupture also remains localized. Affected hatchlings may continue to ail for a long time before dying. Because of the peritonitis and attachment to abdominal wall and intestines, surgical removal of the yolk-sac may not be successful in such cases.

Displacement of the yolk-sac A 3-month-old hatchling Nile crocodile with a non-resorbed and semisolidied yolk-sac was apparently stepped upon by an attendant and, as a consequence, suffered a diaphragmatic hernia which ruptured both the pre-hepatic and the post-hepatic transverse membranes (see p. 12) and displaced the yolk-sac into the right pleural cavity, while the fat body came to lie between the right lobe of the liver and the body wall (Fig. 4.4). The case occurred at a time when there was a high incidence of non-resorption of

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Fig. 4.4. Nile crocodile hatchling with diaphragmatic hernia of the yolk-sac: f, fat body; l, right liver lobe; y, yolk-sac.

yolk-sacs on the farm (Huchzermeyer, 1993). A similar case of diaphragmatic hernia with the yolk-sac projecting into the pleural cavity has been reported by Youngprapakorn et al. (1994), who presumed the case to be due to incomplete closure of the transverse membranes.

Hatchling Diseases
Enteritis

high and necessitate hygienic measures such as periodic cleaning and disinfection. Frequently this creates a situation where only one bacterial species is able to survive, or where initial colonization of the intestine takes place only after feeding with raw meat, particularly if raw minced meat from farm mortalities is being fed, which can introduce many pathogens foreign to the normal intestinal ora. Factors involved

Competitive exclusion In a normal crocodile, even a hatchling, the intestine is protected by a normal intestinal bacterial ora (see p. 38). These bacteria occupy all the available attachment sites on the inner lining of the intestine and thereby prevent pathogenic bacteria from being able to attach. This phenomenon is known as competitive exclusion. In the wild, the normal gut inhabitants are recruited from the nest as well as from the water in the nursery, while contamination with unwanted bacteria is kept at a low level because of the normally low population density of crocodiles in the breeding area. Under the intensive production conditions on the farm, contamination levels are

The presence of such pathogenic bacteria is necessary for an outbreak of enteritis to occur, while the lack of a normal intestinal ora is the major predisposing factor. In addition, temperature stress or other stressors are needed to trigger the outbreak by reducing the resistance and immunity of the hatchlings. Hatchling enteritis therefore must be regarded as a multifactorial disease (see also p. 226). Pathophysiology The inammation of the intestine follows the normal pattern of reptilian inammation with the exudation of brin. The brin lls the intestine and causes an intestinal occlu-

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sion (Figs 4.5 and 4.6). For this reason diarrhoea is rarely seen. Sometimes sheets of brinous pseudomembranes are excreted, particularly in older juveniles and if the condition is not so severe. Intestinal occlusion means that the hatchlings cannot eat and digest any more. They lose weight and become emaciated with an extended abdomen (Fig. 4.7). The diagnosis includes the isolation of the causative bacterium and an antibiogram. Treatment and prevention Because of the intestinal occlusion there is no individual treatment that could be successful. Antibiotic therapy based on the antibiogram established in the laboratory will reach those hatchlings that do not yet suffer from occlusion, and it will prevent the spread of the infection to other hatchlings in the pen. Regular (daily) water changes, as well as scrubbing and disinfection of the oor, are very important preventive measures (see p. 113). A sealed oor surface, either epoxy resin or tiles, allows the cleaning to be more efcient. Fat, leaching from the meat and forming a lm on the surface of the water, is deposited on the oor every time the water

is drained. Here it forms a protective layer under which bacteria can survive ordinary cleaning and disinfection. This fat layer has to be removed from time to time by using a suitable detergent. As the water from crocodile farms is released back into nature, the detergent used should be biodegradable. The use of probiotics and gut ora preparations for hatchling crocodiles has not yet been explored, but can be expected to be of great benet. Heat sterilizing (boiling) the minced meat greatly reduces the challenge by food-borne pathogens (Huchzermeyer, 1991a). Feeding pelleted feeds instead of wet rations has a similar effect. A preventive antibacterial (antibiotic) treatment regime should be avoided because of the danger of the bacteria developing antibiotic resistance, as well as because of environmental implications as the efuents are released back into natural waters (see also pp. 91 and 102).

Alligator hatchling syndrome Alligator hatchling syndrome (AHS) has been described in American alligators (Cardeilhac, 1986; Cardeilhac and Peters, 1988) but is also seen in hatchlings of other

Fig. 4.5. Intestine of a Nile crocodile hatchling lled with, and occluded by, brin.

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Fig. 4.6. Cross-section of an intestine with exudative enteritis and occluded by the exudate.

Fig. 4.7. Emaciation and extended abdomen in a Nile crocodile hatchling suffering from intestinal occlusion due to exudative enteritis.

crocodilian species. Under various conditions of stress (such as cold, overheating, overcrowding, handling and disturbance) opportunistic, normally present, but noninvasive bacteria invade the blood circulation and various organs and seriously affect growth performance and survival, producing a large proportion of runts. The highest incidence is seen in hatchlings under 90 days of age, but juvenile and older crocodiles are also susceptible to stress septicaemia (Huchzermeyer, 2001) (see also p. 228). Virginiamycin and oxytetracycline given continuously for the rst 90 days of life were

both found to be effective in improving the performance and reducing the mortality of hatchlings from hatchling alligator syndrome (Cardeilhac, 1986; Cardeilhac and Peters, 1988). Oxytetracycline was given at a dose of 300 mg kg 1 of feed. However, the continuous use of antibiotics creates the danger of antibiotic resistance and should therefore be avoided if at all possible. Rather, a much more rational approach should be taken along the line of stress prevention by management measures, e.g. protection of the hatchlings against temperature uctuations and extremes. Another approach would be

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via the suppression of stress, e.g. by the continuous use of vitamin C (see p. 278).

Anorexia Under stress-free conditions and at an optimal environmental temperature, crocodile hatchlings will start eating whatever is offered, minced meat or pellets, very soon after hatch. However, at inadequate temperatures, or when subjected to temperature variations, they will not be attracted to inert food. If they do not start feeding by the time the yolk-sac is resorbed, or earlier if resorption of the yolk is prevented by infection (see p. 142), the animals develop a hypoglycaemia which then further depresses the appetite. Although it has been speculated that the affected hatchlings might involuntarily take in some of the minced meat washed into the water, this is unlikely to have any effect (Peucker and Mayer, 1995). The starving hatchlings become emaciated, but may take a long time to die because of their low metabolic requirements. They also develop a hypoproteinaemia, which produces the post-mortem lesions hydropericardium and ascites (Matushima and Ramos, 1993) (see also pp. 234 and 282). If treated early, the condition can be turned around. The treatment consists of force-feeding with a nutrient-rich liquid (a mix of equal parts of milk and egg yolk with some sugar), 1 ml per animal daily for 3 days (my own formula), injecting the hatchlings with glucose solution and possibly also with a multivitamin preparation (Peucker and Mayer, 1995), or the administration of a single dose of metronidazole (Flagyl), 125250 mg kg 1 (Thurman, 1990). Prevention is more likely to be successful. For this the importance of a stress-free rearing environment and adequate temperature control must be emphasized again and again. The appetite can be stimulated by the presentation of live food, such as blood worms spread over the mince or live sh (guppies) (Peucker and Mayer, 1995). Such live food would also serve as a source of normal intestinal bacteria needed for the prevention of enteritis (see p. 145). In an

open-air facility, or one with open windows, an electric light suspended high above each rearing pen will attract ying insects at night which, when falling down, are caught by the hatchlings even before they hit the water (see p. 109).

Osteomalacia If hatchlings are fed mince without bone, e.g. minced meat of large animals, and particularly liver and heart, they develop a calcium and phosphorus deciency which prevents the hardening of the growing bones. Affected hatchlings remain able to move freely in the water, but have difculty to move on land and eventually will be unable to come out of the water. Contraction of the long muscles of the back causes the vertebral column to become deformed. The upper jaw becomes exible and can be bent upwards (rubber jaws) and the teeth become diaphanous, like shards of glass (glassy teeth) (Huchzermeyer, 1986). The treatment consists in the supplementation of the ration with calcium and phosphorus in the form of bone meal or calcium diphosphate, or feeding mince of whole small animals (poultry) minced with the bones. However, the deformities of the vertebral column will remain (Huchzermeyer, 1986). For a more detailed description of this condition and discussion of its causes see Chapter 6.

Congenital Malformations
Congenital malformations are caused from time to time by mishap when something goes wrong in one or other of the developmental processes. Such a mishap will cause a single case. Ferguson (1989) found an increased incidence of malformations in hatchlings from very young and very old females. If there is an increased incidence of any particular type of malformation, one will have to consider genetic causes, malnutrition of the parents or faulty incubation. Mutated genes may be recessive and remain inapparent until both parents in a mating carry the

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same mutated gene. Therefore one would expect a low incidence of such cases but repeatedly, year after year, and limited to one or two clutches. A blind gene has been suspected to occur in natural gharial populations in Nepal (Singh and Bustard, 1982). Malnutrition of the parents would affect the majority of the hatchlings, and the lack of certain vitamins is also suspected to play a role in the causation of deformities in crocodilian embryos. The effect of malnutrition on the incidence of shell defects has been dealt with above. Incubation errors may happen only once during an incubation period and may affect many clutches at different stages of incubation in the same incubator in different ways, depending on the stage of incubation, thus producing a range of malformations in different clutches for one incubation season. Continuous incubation at the limits of the viable range of incubation temperatures (29 or 34C) has been reported to produce a high incidence of malformations in American alligator embryos (Ferguson, 1989). Webb and Manolis (1998) state that high-temperature incubation (35C), particularly in the early stages, causes various spine abnormalities, strongly curled tails, skull deformities by inducing premature ossication and also protruding lower jaws in C. porosus and Crocodylus johnsoni hatchlings. Many congenital defects are lethal, killing the embryo or the hatchling shortly

before or after hatch. Where hatchlings with defects survive, particularly in nature, and are found later, their defects may be confounded with healed injuries. From a practical point of view, the details of congenital malformations are of lesser importance and more of curiosity value. However, the attention of the reader is directed to the excellent photography of congenital malformations in the book by Youngprapakorn et al. (1994).

Axial and tail deformities Many different deformities of the vertebral column have been reported from different crocodilian species, and they affect different parts of the spine. Necks bent sideways have been reported from gharial hatchlings (Singh and Bustard, 1982). Scoliosis and kyphoscoliosis (humpback formation) of the spine has been reported by Ferguson (1989) and Hibberd (1996). The tail can be affected by a number of different deformities, such as a permanent sideways bending, a sharp kink (Figs 4.8 and 4.9), curling (Fig. 4.10), shortening or complete absence (Figs 4.11 and 4.12) (Kar and Bustard, 1982b; Singh and Bustard, 1982; Ferguson, 1989; Youngprapakorn et al., 1994; Hibberd, 1996; Troiano and Romn, 1996; Webb and Manolis, 1998). Tailless crocodiles cannot swim and will drown once they go into deep water.

Fig. 4.8. Kinky tail in a Nile crocodile hatchling.

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Fig. 4.9. Gharial hatchling with a kinky tail.

Fig. 4.10. Nile crocodile hatchling with a curled tail.

Fig. 4.11. Juvenile Nile crocodile born without a tail.

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Fig. 4.12. Tailless Osteolaemus tetraspis hatchling.

A spina bida has been reported by Ferguson (1989).

Polydactyly and limb duplication Functional additional toes, some with and some without claws, three on each front foot and three and four on the hind feet, were found in an 82-cm-long wild American alligator in Louisiana (Giles, 1948). A case of non-functional polydactyly and syndactyly has been reported by Youngprapakorn et al. (1994). Similar cases were seen in South Africa in Nile crocodile hatchlings from one particular farm (Figs 4.13 and 4.14) (own cases).

The duplication of limbs is one of the malformations believed to be caused by incubation at extreme temperatures (Ferguson, 1989). An adult Nile crocodile with an additional pair of hind limbs is shown in Fig. 4.15. Youngprapakorn et al. (1994) show a hatchling with one additional limb attached to the navel and bearing a single clawed toe, which may, however, have been an incomplete twin (see p. 153).

Ectromelia and micromelia The complete absence of one foreleg, on radiographs even the absence of the shoulder blade, was found in two wild Crocodylus

Fig. 4.13. Nile crocodile hatchling with polydactyly of both left limbs as well as left anophthalmia.

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Fig. 4.14. Polydactyly and syndactyly in a Nile crocodile hatchling.

Fig. 4.15. Adult Nile crocodile with an additional pair of hind limbs attached to its back.

moreletii, of a total length of 37 cm and 104 cm (Rainwater et al., 1999). Youngprapakorn et al. (1994) show a hatchling with both forelimbs missing and also mention cases with shortened legs, micromelia. Missing limbs are also listed amongst congenital malformations of caiman hatchlings (Troiano and Romn, 1996).

Malformations of head, jaws and eyes Hall (1985) reported cases of brachycephalic (shortened) skulls and dental anomalies in

New Guinea crocodiles. The dental anomalies included supernumerary and subnumerary dental counts, double sets of teeth erupting from a single alveolus and alveolar ossication, which the author did not believe to be an expression of the ageing process. Brachycephalic skulls have also been found in other crocodilian species: A. mississippiensis, Crocodylus niloticus and C. porosus (Klin, 1936). Unilateral anophthalmia, monophthalmia, causes an asymmetric development of the skull (Youngprapakorn et al., 1994). Bumps, tubercles, on top of the skull, as shown by Youngprapakorn et al. (1994), are

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believed to be caused by premature ossication of the skull in hatchlings incubated at too high a temperature (Webb and Manolis, 1998). Monorhiny, the formation of a single nasal passage, was reported by Ferguson (1989). The lower jaws can either be protruding or shortened or missing completely, agnathia (Ferguson, 1989; Youngprapakorn et al., 1994; Hibberd, 1996). Protruding lower jaws commonly occur in C. johnsoni hatchlings and are believed to be caused by high-temperature incubation (Webb and Manolis, 1998). A slightly protruding upper jaw causes the two large incisor teeth of the short lower jaw to penetrate through the apical maxilla, producing false nostrils (see Fig. 1.21). Sideways bending of the upper jaw of a monophthalmic gharial hatchling was reported by Singh and Bustard (1982), and upwards curving of the snout in wild C. johnsoni by Webb and Manolis (1983). Cleft lip, cleft palate and cleft chin are shown by Youngprapakorn et al. (1994). Sideways bending of the lower jaws (Fig. 4.16) may also be caused by injury later in life (see also p. 95). Reported malformations of the brain include hydrocephalus and meningo-encephalocele (Ferguson, 1989; Youngprapakorn et al., 1994; Hibberd, 1996; Webb and Manolis, 1998). Malformed eyes can be too small

(microphthalmia), completely missing (anophthalmia) on one or both sides (see Fig. 4.13), protruding (exophthalmia) or moved to the front of the head (cyclopia) (Singh and Bustard, 1982; Millichamp et al., 1983; Jacobson, 1984; Ferguson, 1989; Youngprapakorn et al., 1994; Hibberd, 1996). Defects of cornea and iris and the sealing of the nictitating membrane (third eyelid) have also been reported (Singh and Bustard, 1982; Youngprapakorn et al., 1994).

Twins Twins can be either monozygotic (identical twins), originating from one ovum (germ cell and yolk-sac) or dizygotic, originating from separate ova included in one egg (doubleyolked egg). Double-yolked eggs are larger than the other eggs in the clutch. However, the embryos remain small and usually die before hatching, or, if they hatch, fail to develop normally and remain stunted (Blomberg, 1979; Hibberd, 1996; Webb and Manolis, 1998). Elongated eggs containing three yolks have also been reported (Youngprapakorn et al., 1994). This can happen when the simultaneously ovulated yolks travel down the oviduct too closely to one another.

Fig. 4.16. Adult captive Crocodylus porosus with skewed jaws.

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Monozygotic twins occur more frequently than dizygotic ones (Youngprapakorn et al., 1994). They share one yolk-sac and therefore either die when they both fail to internalize the yolk-sac or become attached to each other at the navel. The surgical separation of such omphalopagous twins may be very difcult because of the shared yolk-sac (Larriera and Imhof, 1994; Youngprapakorn et al., 1994). Incomplete twinning occurs when the separate development of the two monozygous embryos has occurred at a slightly later stage and one of the twins has remained incomplete. Such incomplete twins may have two heads on one body or may be joined at various parts of the body, as Siamese twins (Ferguson, 1989; Youngprapakorn et al, 1994; Troiano and Roman, 1996), or the incomplete twin may consist of a limb or even incomplete limb only, which is attached to the navel of the other twin (Fig. 4.17).

Albinism and other colour variations Albinism consists of the complete absence of pigment in skin and eyes, producing a white skin and red eyes. Sometimes the transverse markings can be seen as faint shadows. Crocodile farmers often refer to any white or light-coloured crocodiles as albinos, but this

is incorrect. True albino crocodiles are quite rare but have been found in caiman and American alligators (Allen and Neill, 1956; Troiano and Romn, 1996). True Nile crocodile albinos have also hatched from time to time on a particular farm in South Africa. White crocodiles with dark markings are not albinos and the condition is not partial albinism but rather leucotism. Such animals, also called leucystic, have pigmented eyes which are blue-grey, and a white skin with darker markings when young, but the skin becomes darker as the animals mature (Kar and Bustard, 1982a; Barnett et al., 1999). Unfortunately Bezuijen (1996) does not describe the eye colour of the albino crocodiles in Cambodia. Their dark markings suggest that they are merely white. A melanistic (black) spectacled caiman hatchling from Colombia had black eyes and only a narrow greyish area along its ventral midline (Allen and Neill, 1956). An erythrystic (red) American alligator had reddishbrown cross bars over a normally coloured background (Allen and Neill, 1956). American alligator embryos incubated at an elevated temperature (33C) develop one extra transversal stripe. This is due to the large size of the embryo at the stage when the wave-like pattern of pigmentation initiation passes down the body of the embryo (Ferguson, 1989).

Fig. 4.17. Incompletely formed homozygous twin attached to the navel of the completely formed Nile crocodile hatchling.

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Abdominal wall defects Several defects of the walls of thorax and abdomen have been described by Youngprapakorn et al. (1994). These include non-closure of the thorax with ectopic heart, non-closure of the abdominal wall with ectopic yolk-sac and intestines, and non-closure of the abdominal wall between navel and cloaca. Ectopia cordis has also been found in an American alligator hatchling (Elsey et al., 1994).

ally led to the death of the hatchling. My own observations in farmed Nile crocodiles include extra loops on the duodenal loop (Figs 4.18 and 4.19), which appears to be relatively common, doubling of the gall bladder, one in each liver lobe and each with a separate duct leading into the duodenum (Fig. 4.20), and a twolobed fat body (Fig. 4.21). None of these latter malformations appeared to have any serious effects on the crocodiles.

Congenital gout Malformation of internal organs The reported congenital defects of internal organs include oesophageal stenosis, duodenal atresia and atresia of the bile duct (Youngprapakorn et al., 1994). In all these cases the closure of the important passages eventuNon-formation of one kidney has been seen in our own post-mortem material. In such cases, the remaining kidney showed compensatory growth. It is not clear whether the congenital gout described by Foggin (1992a) was cause by an absence of kidney formation or by non-functional kidneys.

Fig. 4.18. Malformed duodenal loop in a juvenile Nile crocodile: extra twist.

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Fig. 4.19. Malformed duodenal loop in a juvenile Nile crocodile: extra arm.

Fig. 4.20. Double gall bladder in a juvenile Nile crocodile, the right liver lobe has been removed.

Fig. 4.21. A two-lobed fat body in a Nile crocodile.

Chapter 5
Transmissible Diseases

Transmissible diseases are those caused by infectious or parasitic agents, including parasitic infestations. There are several crocodilespecic viral and bacterial infections, some of which may even be species or genus specic. However, their present distribution may also be due purely to geographical limits. The specicity of parasites also varies. In addition, there are many non-specic infections, particularly bacterial and fungal. Contamination and infection have to be seen in quantitative terms. While a low infection pressure may not sufce to overcome the defences of the host, the build-up of contamination in an intensive rearing unit may reach such proportions as to be able to overcome even high levels of immunity. In addition, the immune-suppressive action of stress may in fact trigger outbreaks of infectious diseases, if the infectious agent is already present in the rearing pens. In other words, the presence of poxvirus, chlamydiae or coccidia alone is not enough to start an outbreak of the disease, one or more triggering factors may be needed to allow the infection to manifest itself as disease.

The diagnosis of viral infections should be based on the presence of specic pathological and histopathological lesions, possibly with typical inclusion bodies, on electron microscopy, on serological tests and on the isolation and characterization of the virus. With regard to crocodile viruses, there is a serious problem. None of them can be isolated in embryonated chicken eggs, the most common tool in veterinary virology laboratories, nor can they be grown in any of the cell culture lines presently in use. Nobody has yet isolated or established crocodile embryonic cell lines that could be used for this work (see Notes Added at Proof, p. 210). Such viral cultures are also necessary for the preparation of antigens for serological tests, as well as for the manufacture of specic vaccines. Without the ability to grow crocodile viruses in cell culture, we still are lacking some very important tools. It is amazing that a book on reptile medicine and surgery published as recently as 1996 by a reputable publishing house can contain a statement to the effect that the only known viral disease of crocodiles was caiman pox (Lane, 1996). Caiman pox Caiman pox is the infection with a Parapoxvirus and is characterized by grey or
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Viral Infections
Unlike ostriches, crocodiles have their own specic infectious diseases, amongst them pox and adenoviral hepatitis, but they can also acquire infections from other animal species.

CAB International 2003. Crocodiles: Biology, Husbandry and Diseases (F.W. Huchzermeyer)

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greyish-white lesions in the mouth and on the dorsal skin of the head, body and legs of hatchling and juvenile spectacled caimans. Outbreaks have been reported from the USA (Jacobson et al., 1979), Hungary (Vetsi et al., 1981), South Africa (Penrith et al., 1991), Brazil (Matushima and Ramos, 1993, 1995; Cubas 1996) and Colombia (Villafae et al., 1996). The colour and distribution of lesions and the limitation of the disease to probably one single species of Caiman indicate that this is a separate disease entity. Outbreaks of clinical disease usually occur in hatchlings and juveniles under 1 year of age and may affect a large proportion of the animals being reared together. The infection appears to be limited to Caiman crocodilus. Some authors state that the animals recover after a prolonged period without apparent ill effects (Cubas, 1996), while others report severe clinical problems, including retarded growth and eventual death (Vetsi et al., 1981). This may depend on conditions in the rearing environment. Complete recovery may take 6 weeks or longer. The lesions in the oral mucosa and on the dorsal skin of head, body and legs begin as small, round, whitish papular lesions 1 mm in size and usually situated between scales. Later they become covered with greyishwhite crusts, increase in size, become conuent, assume irregular shapes and cover one or even several scales (Plate 7). Microscopically the lesions are characterized by epithelial hyperplasia, acanthosis, hyperkeratosis and necrosis. Enlarged epithelial cells contain large, deeply eosinophilic cytoplasmic inclusions, which are typical Bollinger bodies or smaller inclusions (Borrel bodies). Transmission electron microscopy reveals these inclusions to contain large numbers of dumb-bell-shaped virions (Jacobson et al., 1979). Negatively stained preparations of the caiman poxvirus revealed the regular criss-cross surface pattern characteristic of the genus Parapoxvirus, similar to those of the crocodile poxvirus (p. 160) (Gerdes, 1991). Attempts to isolate the virus on various reptile cell lines have failed (Jacobson et al., 1979). It is believed that individual caimans can carry and shed the virus without being clini-

cally affected. This shedding can take place either on the farm or in a natural population in the vicinity of the farm, from which the virus can be introduced into the rearing facility by the use of water from the river or lake inhabited by the wild population. There is also evidence that stress may play a role in triggering actual outbreaks, if the virus is present already. There is no specic treatment. Providing optimal rearing conditions and good food will help to speed up the recovery. There is no further experimental evidence that natural or articial sunlight will improve chances of recovery as stated by Penrith et al. (1991). Prevention consists of providing a stress-free rearing environment, strict hygiene, including the regular scrubbing and disinfection of the rearing pens, and the use of borehole or well water for the rearing units, instead of river water.

Crocodile pox Crocodile pox is an infection of hatchling and juvenile crocodiles with a Parapoxvirus, characterized by brown crusty lesions in the oral cavity, on the head and on the ventral and lateral surfaces of the body and tail. Outbreaks of the disease have been reported in Nile crocodiles (Foggin, 1987; Horner, 1988a; Pandey et al., 1990; Huchzermeyer et al., 1991; Buoro, 1992) and individual cases in C. porosus and C. johnsoni (Buenviaje et al., 1992, 1998b; Turton et al., 1996). The colour of the lesions, their distribution on the ventral and lateral aspects of the body and the apparent limitation of the infection to a small range of Crocodylus species indicate that this is a separate disease entity. Outbreaks of clinical disease occur in hatchlings as well as juveniles under 2 years of age. Small (13 mm) sunken or prominent and crusty brown lesions appear on the head and on the ventral and lateral surfaces of body and tail, often apparently associated with bite marks (Plate 8) (Huchzermeyer et al., 1991). Lesions on the eyelids may cause blindness, and lesions on the head may cause a shrinking of the skin, leading to

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deformities (Foggin, 1987; Horner, 1988a). While the morbidity is high, mortality usually remains low, unless the disease becomes complicated by opportunistic bacterial and fungal infection of the lesions. Recovery is normally spontaneous within a few weeks or months. The pathology is limited to the skin lesions as described above. Microscopically the lesions are characterized by hyperkeratosis and parakeratosis with ballooning epithelial cells containing single large intracytoplasmic inclusions (Bollinger bodies) or several small inclusions (Borrel bodies) (Fig. 5.1). Unlike avipox lesions, the inclusions of crocodilian pox cannot be stained with a fat stain. By electron microscopy numerous dumb-bell-shaped virions can be demonstrated, which have been identied in negatively stained preparations, by their crisscross striations, as belonging to the genus Parapoxvirus (Fig. 5.2) (Gerdes, 1991). Attempts to grow the virus in embryonated chicken eggs and on chicken cell lines have failed (Horner, 1988a). It is presumed that the virus can be carried and shed by clinically healthy carriers. In one case, the disease was introduced presumably with the acquisition of hatchlings from a farm where the disease had occurred previously (Horner, 1988a). Wild crocodiles

in the vicinity of a crocodile farm probably are the most common source of infection, which can enter the farm with the water from the river or lake harbouring a wild population. Adult breeding stock on the farm also are a possible source of the virus. While the virus could possibly be transmitted by mosquito bite, it is much more likely to be transmitted by contaminated water. Stress must be seen as the major factor triggering outbreaks in the presence of the infection. There is no specic treatment against crocodile pox infection, although secondary infections may warrant therapeutic intervention. Attempts at individual treatment and the associated handling may cause stress and negatively affect the individual animals (Horner, 1988a). A crude autogenous vaccine prepared from scabs from affected animals reduced the recovery time (Horner, 1988a), but there is the danger of causing generalized infection amongst unvaccinated individuals, when the live vaccine virus is introduced into the rearing environment (Foggin, 1992a). The prevention of crocodile pox infection is based on avoiding the use of potentially contaminated water rather use borehole or well water in the rearing section and the avoidance of stress, particularly heat stress.

Fig. 5.1. Crocodile pox lesion with intracytoplasmic inclusions.

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Fig. 5.2. Transmission electron micrograph of crocodile pox virus particles, showing the criss-cross surface striations (micrograph G.H. Gerdes).

Adenoviral infection Adenoviral infection most commonly affects the liver of Nile crocodile hatchlings under 5 months of age, less often the intestines and pancreas, and sometimes the lungs as well, but rarely all in the same animal (Jacobson et al., 1984; Foggin, 1987, 1992a,b). The disease occurs mainly in Zimbabwe but has been diagnosed in South Africa as well. Adenoviral particles were found by transmission electron microscopy in negatively stained faeces of three Nile crocodile (length 3147 cm), which had been imported to South Africa from Mozambique (Fig. 5.3) (Huchzermeyer et al., 1994b). In experimen-

tal transmission trials by oral administration of naturally infected liver, the incubation period was 218 weeks (Foggin, 1992a). There is a suspicion that it may also be transmitted vertically via the egg from mother to hatchling, although horizontal transmission appears to be more common (Foggin, 1992a). Successful isolation of the crocodile adenovirus virus has never been reported. Apart from lethargy and anorexia, there are no clinical symptoms. Sometimes the infection is associated with the occurrence of massive mortality, particularly during the winter months. However, other factors may be involved in these outbreaks (Foggin, 1987). The virus frequently causes a chronic

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Fig. 5.3. Transmission electron micrograph of a crocodile adenovirus particle (micrograph J.F. Putterill).

hepatitis which, in Zimbabwe, is seen as a major cause of runting (Foggin, 1992b). On post-mortem examination, there may be slight icterus. The liver is markedly swollen and pale (Fig. 5.4) and the bile is pale yellow instead of the normal dark-green colour (Foggin, 1992a). The intestine may be swollen and congested, and is sometimes lled with brinous exudate. The infection is conrmed histopathologically by the demonstration of the typical intranuclear inclusion bodies in the hepatocytes of the liver, the intestinal or pulmonary epithelium, or the acinar cells of the pancreas (Fig. 5.5) (Jacobson et al., 1984; Foggin, 1992a). Common ndings in chronic adenoviral

hepatitis are brosis of the portal tracts and bile duct hyperplasia (Foggin, 1992a). There is no treatment for the infection, although antibiotic treatment of the secondary bacterial infections may have a benecial effect in serious outbreaks. In the absence of a suitable medium for the isolation of the virus, it is impossible to produce a vaccine. Prevention should be based on strict hygienic measures aimed at preventing the horizontal spread of the virus, including not using water from rivers inhabited by wild crocodiles, and preventing stress, particularly thermal stress caused by wide temperature uctuations in open-air rearing pens in winter.

Fig. 5.4. Nile crocodile hatchling with adenoviral hepatitis.

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Fig. 5.5. Intranuclear adenoviral inclusion bodies in the pancreas of a Nile crocodile hatchling.

Newcastle disease paramyxovirus The Newcastle disease virus does not cause clinical disease in crocodiles, but Nile crocodiles fed fowls that had died from Newcastle disease were found to seroconvert (Thomson, 1972). Paramyxovirus particles, believed to be Newcastle disease virus, were found by transmission electron microscopy in negatively stained faeces of crocodiles (length from 32 to 144 cm) from a farm where the crocodiles had been fed with dead chickens from a poultry farm on which an outbreak of Newcastle dis-

ease had occurred (Fig. 5.6). A paramyxovirus was also found in the faeces of a single crocodile from a farm where no poultry had been fed (Huchzermeyer et al., 1994b). Seroconversion takes place only if the virus multiplies within the host. Excretion of the virus in the faeces could mean that crocodiles can act as carriers and a possible source of infection for wild waterbirds. In a recent serological survey, wild waterbirds were found to be a potential reservoir of Newcastle disease virus in South Africa (Ptzer et al., 2000).

Fig. 5.6. Paramyxovirus in negatively stained faeces of a farmed Nile crocodile that had been fed dead chickens from an outbreak of Newcastle disease (micrograph J.F. Putterill).

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In the light of the above, there is a strong suspicion that the outbreaks of conjunctivitis and encephalitis reported from farmed caimans in Colombia (Villafae et al., 1996) could also be caused by a paramyxovirus (see also p. 245).

may not have contributed to the high mortality rate (Huchzermeyer et al., 1994b). Coronavirus Coronavirus-like particles were found by transmission electron microscopy in negatively stained faeces of four 23-year-old crocodiles from a farm with severe mortality in that age group (Fig. 5.8). They were present in very high concentrations in two of the four specimens (Huchzermeyer et al., 1994b). It is not possible to say whether this agent was pathogenic and contributed to the high mortality, or whether it was only opportunistic and able to multiply in severely compromised animals. See Notes Added at Proof, p. 210.

Eastern encephalitis virus Antibodies to the virus of eastern equine encephalitis (EEE) were found in the blood of a single American alligator, adding this species to the list of possible reptile carriers of the virus (Karstad, 1961; Lunger and Clark, 1978; Jacobson, 1984). The carrier reptiles are not affected clinically by the infection.

Inuenza C virus

Bacterial Infections
Filamentous forms of inuenza C virus were found by transmission electron microscopy in negatively stained faeces of eight Nile crocodiles (length 3181 cm) from one farm associated with high mortality over a period of 1 month (Fig. 5.7). The animals had been exposed to severe stress caused by overstocking, handling and uctuating temperatures, which could have rendered the animals more susceptible to the infection, which may or Only a few bacteria cause specic diseases in crocodiles, and even fewer of these are crocodile-specic. However, very many different species of bacteria can cause nonspecic septicaemias. These bacteria are recruited either from the aquatic environment, the intestinal ora or from food contaminants, particularly where raw meat is used as feed.

Fig. 5.7. Inuenza C virus in negatively stained Nile crocodile faeces (micrograph J.F. Putterill).

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Fig. 5.8. Coronavirus-like particles in negatively stained faeces of a farmed Nile crocodile (micrograph J.F. Putterill).

All septicaemias, specic and non-specic, are triggered, if not caused, by stress. Bacteria are allowed to escape under severe stress from the intestine into the blood circulation (see p. 228), and if the stress continues, the resultant immune suppression prevents the crocodile from overcoming the initial escape and allows the bacteria to gain a foothold. Infections in septic wounds normally are contained by briscess formation, the exudation of brin into the septic area, which immobilizes the invading bacteria (see p. 46) (Huchzermeyer and Cooper, 2000). Identifying and eliminating the source of stress that has triggered an outbreak of septicaemia is the most important part of the treatment in an outbreak of bacterial infections, as antibacterial treatment alone is rarely successful. The elimination of potential stressors and the identication of potential sources of infection play a major role in all prophylaxis programmes. Salmonellosis Salmonellosis is caused by bacteria of the genus Salmonella and manifests itself either as enteritis, particularly in hatchlings (see p. 145), or as septicaemia. This is not a crocodile-specic disease, as the agents can infect many different animal species, and some of the salmonellae, particularly S. enteritidis and

S. typhimurium, are also human pathogens. Crocodiles, like other reptiles, harbour salmonellae in their intestines as part of their normal gut ora. Bacteriologists and veterinarians become excited whenever salmonellae are found. However, the danger of any of these salmonellae spreading to people is minimal. How many records are there of human salmonella infections originating from crocodiles? Species and serovars of Salmonella that have been isolated from crocodiles are listed in Table 5.1. Bacterial septicaemia is often precipitated by severe stress, particularly temperature stress such as overheating or frequent temperature changes (pp. 228 and 278). In these cases the salmonellae act only as opportunistic invaders, similarly to many other bacteria. The ongoing infection may cause depression and anorexia. In advanced cases the bacteria may attack the joints, taking the form of polyarthritis, which renders the affected crocodiles unable to move (see p. 273). The enteritic form of the disease may either cause brinous exudation and occlusion of the intestine (see p. 145) or diarrhoea, sometimes with portions of brinous casts (pseudomembranes) in the faeces. A haemorrhagic enteritis due to S. choleraesuis has also been described (Ocholi and Enurah, 1989). The clinical diagnosis can be established only on the strength of bacterial cultures of blood, faeces or synovial aspirate. The postmortem ndings are non-specic and need

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Table 5.1. Salmonella serovars isolated from crocodiles. Serovar Salmonella I Rough Untypeable 9,12:1; v:17:Z4Z23Z32 Aarhus Aberdeen Abony Adelaide Agama Agodi Agona Agoueve Alamo Albany Anatum Antarctica Arechavaleta Bahrenfeld Banana Bangui Binza Blockley Bonn Bovis-morbicans Braenderup Brancaster Brazos Bredeny Brisbane Bron Budapest California Cerro Chester Chicago Choleraesuis Cullingworth Dabou Derby Diguel Duesseldorf Duval Eastbourne Edinburgh Emek Enteritidis Farsta Good Haardt Havana Herston Reference Serovar Salmonella I (continued) Infantis Israel Javiana Johannesburg Kinondoni Kingston Kisangani Kottbus Koumra Livingstone Montevideo Muenchen Naestved Ndolo Newport Newlands Onderstepoort Oranienburg Orion Os Oslo Othmarschen Phaliron Plymouth Poona Ried Saint-Paul Sandiego Schwarzengrund Schwerin Senftenberg Shamba Simi Singapore Soa Somone Tallahassee Tanger Tennessee Thompson Tinda Tsevie Tshiongwe Typhimurium Reference

1 1, 4, 9 2 1 1 1 2 1, 2, 4, 9 1 1 2 1 1 1 1, 2, 4, 17 1 1 17 2 1 4 1 10 17 1 1 1 2 1 1 1 1 4 4, 17 2 7 2 1 11 1 1 1 2 2 2 4 1 1 1 4 1

Urbana Virchow Wagenia Wangata Waycross

2, 4 1 1 2, 5, 6, 17 4 1 1 2 9 4 2 2, 4, 14 1 1 2 1 17 2 2, 4 1 1 1 1 2 4, 15, 17 1 2, 4, 15 1 1 1 2, 4 13 1 4, 17 4 1 1 1 4 4 1 1 1 1, 2, 4, 5, 6, 9, 12, 16, 17 17 17 1 1 5 Continued

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Table 5.1. Continued. Serovar Salmonella I (continued) Weltevreden Westhampton Yaba Yoruba Salmonella II Rough 6,8; eh; enz15 9,12; gz62; 16; gt; z42 16; z; enx 39; mt; enx 40; b; 48; k; enxz15 55; -; Salmonella III Untypeable 16:z10:e,n,x,z15 48:1;v; z35 50; -; 50; k; z Reference Serovar Salmonella IIIa 48; k; z53 Salmonella IIIb 28; -; 30; k; enx 38; k; z35 48; k; z53 48; r; enxz15 50; r; z35 50; r; z53 50; z52; z35 60,65; k; z Salmonella IV 50; z4z23 Group C Group D Group E Group 5 S. arizona Reference

4 1 1 1

1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1

1 9 9 9, 10 8, 9 3, 4, 5, 8, 9, 11, 17

1 14 2 1 17

References: 1, Van der Walt et al. (1997); 2, Greenberg and Sechter (1992); 3, Ippen (1965); 4, Manolis et al. (1991); 5, Ladds and Sims (1990); 6, Hibberd et al. (1996); 7, Ocholi and Enurah (1989); 8, Obwolo and Zwart (1993); 9, Foggin (1992a); 10, Madsen (1993); 11, Foggin (1987); 12, Shotts et al. (1972); 13, Rudat et al. (1966); 14, Habermalz and Pietzsch (1973); 15, Cope et al. (1955); 16, Huchzermeyer (1991a); 17, Millan et al. (1997b).

to be conrmed by bacterial isolation. The treatment of clinical cases comprises oral or parenteral administration of an antibiotic selected by antibiogram and the elimination of the precipitating stressor(s). If the animal still eats, the oral route should be chosen, as parenteral administration may need further physical immobilization of the animal and thereby further stress. On farms, treatment should be aimed at containing the outbreak rather than at saving affected individuals. Administration of a suitable antibiotic in the feed, eliminating the stressor(s) and eliminating the source of infection are of equal importance. However, it should be noted that the salmonellae may have been present in the intestines of some of the animals for a considerable time before the outbreak, and have only become active when stress reduced the resistance of the

crocodiles. Since the spread occurs by the faecaloral route, water changes, scrubbing and disinfection of the pens are of prime importance (see p. 113). The prevention of salmonellosis must be based on the use of sanitary feed (pellets or boiled mince), a strict hygiene programme (smooth surfaces free of cracks, washing with a detergent to remove protective layers of fat, thorough disinfection with each change of water; see p. 113), and the elimination of all stressors, in particular the protection from varying and excessive temperatures. While the use of a calf paratyphoid vaccine in an outbreak of salmonellosis due to S. typhimurium has been reported (Huchzermeyer, 1991a), it is doubtful whether such a vaccination would have any prophylactic value, particularly in view of the plethora of immunologically different Salmonella isolates listed in Table 5.1.

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Mycoplasmosis Cases of polyarthritis in 13-year-old Nile crocodiles have occurred on several farms in Zimbabwe (Mohan et al., 1995) and similar cases have been reported from Israel and Spain (Levisohn and Bernstein, and Oros, both quoted by Mohan et al., 1997). Mycoplasmas were isolated from lungs and synovial uid of the Zimbabwean crocodiles and the isolates were identied as Mycoplasma crocodyli (Kirchhoff et al., 1997). The sick animals had swollen joints and were progressively unable to move. The joints were lled with excessive quantities of turbid uid, in chronic cases with dry brinous exudate, and some of the animals were found to have lesions of pneumonia (Mohan et al., 1995). In an outbreak of mortality in adult male American alligators, Mycoplasma sp. was isolated from lungs and synovial uid from seven out of eight of the euthanized animals (Clippinger et al., 1996). Clinically the animals had been in poor condition, with anorexia, lethargy, muscle weakness, paraparesis, bilateral white ocular discharge and varying degrees of periocular, facial, cervical and limb oedema. The authors referred to the state of these 30-year-old animals as geriatric (Clippinger et al., 1996). Intramuscular treatment with oxytetracycline (10 mg kg 1 estimated body mass) every 7 days for 1 month and every 14 days thereafter for 5 months appeared to have had benecial results. The agent was identied as Mycoplasma alligatoris (Brown et al., 2001a). Experimental infection of American alligators produced fatal disease, with brinous polyserositis, polyarthritis, myocarditis and meningitis (Brown et al., 2001b). Broad-nosed caimans were also susceptible to fatal experimental infection, while Siamese crocodiles were not affected clinically but reacted serologically (Brown et al., 2001b,c). Treatment of the Zimbabwean cases with tetracycline by injection, followed by administration of the same antibiotic in the feed, ameliorated clinical signs but did not prevent relapses (Mohan et al., 1997). A vaccine made from M. crocodyli gave a certain degree of protection (six out of eight) to animals that had received a booster 21 days after the rst vaccination (Mohan et al., 1997).

The epidemiology of this disease still remains unresolved. It is to be presumed that wild crocodiles act as reservoirs of infection. Vertical transmission has been suggested to be the major mode of transmission and this is likely to affect farms with hatchlings from eggs collected from the wild (Mohan et al., 1996). Limited trials in Zimbabwe could not demonstrate the horizontal transmission of the disease to in-contact animals from a farm known to be free from mycoplasmosis (Mohan et al., 1996). However, unidentied mycoplasmas (Fig. 5.9) were found in the faeces of crocodiles from two farms in South Africa, and this nding could demonstrate the mode of excretion for horizontal transmission (Huchzermeyer et al., 1994b). There is no doubt that stress serves as a triggering factor for outbreaks of mycoplasmosis, as with other bacterial infections. Blood cultures from the American alligators yielded a range of bacteria but different bacteria were isolated from different individuals (Clippinger et al., 1996). This is typical for outbreaks of stress septicaemia (see p. 228). Specic enzyme-linked immunosorbent assays (ELISA) for M. alligatoris and M. crocodyli could be used to screen crocodiles before export or import, or before their release back into nature (Huchzermeyer, 2001).

Chlamydiosis Chlamydiosis is a disease in farmed Nile crocodiles caused by chlamydiae closely related to Chlamydia psittaci, but probably a different species. There are two forms: an acute hepatitis and a chronic conjunctivitis (Huchzermeyer et al., 1994a). Chlamydiae were isolated together with mycoplasmas from cases of polyarthritis in Nile crocodiles in Israel (Levisohn, 1995, quoted by Mohan et al., 1996). In Zimbabwe acute chlamydiosis often is found associated with adenoviral hepatitis (Foggin, 1992b). In outbreaks of the acute form, the affected hatchlings die without having shown any signs of illness. On post-mortem examination the liver is found to be pale, mottled and enlarged (Fig. 5.10) and the spleen slightly enlarged (see also p. 270). There is a mild ascites and a severe hydropericardium

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Fig. 5.9. Electron micrograph of a mycoplasma found in negatively stained faeces of farmed Nile crocodiles in South Africa (micrograph J.F. Putterill). Previously published in the OIE Bulletin (Huchzermeyer, 2002).

Fig. 5.10. Nile crocodile hatchling with chlamydial hepatitis and hydropericardium.

(Fig. 5.10). The most severe histopathological changes are found in the liver: a severe portal to diffuse lymphoplasmocytic hepatitis with congestion, mild bile duct proliferation, vacuolar degeneration of the hepatocytes and multifocal to coalescing necrosis. Numerous colonies of intracytoplasmic organisms are present in the hepatocytes (Fig. 5.11). The

chlamydiae in the liver tissue can be stained with special stains or demonstrated in liver impression smears stained with Giemsa stain. The organisms can be isolated in embryonated chicken eggs as well as in tissue culture. The chronic cases, which are more common in South Africa, occur in the form of a bilateral blepharo-conjunctivitis with swelling

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Fig. 5.11. Chlamydial hepatitis in a Nile crocodile hatchling, intracellular chlamydial colonies in the hepatocytes (haematoxylin and eosin).

and increasing opacity of the third eyelid, and nally the accumulation of brinous exudate under the third eyelid, leading to blindness (Fig. 5.12). Such outbreaks can affect up to 50% of the hatchlings or juveniles in a pen. In these cases demonstration of the presence of chlamydiae by microscopy is much more difcult, almost impossible, as only very few are present, but the isolation of the agent in tissue culture or embryonated eggs is more likely to be successful. The agent is sensitive to oxytetracycline and this is administered via the feed:

Terramycin soluble powder (Pzer, oxytetracycline 55 mg g 1) 10 g kg 1 (Foggin, 1992b), or pure oxytetracycline 1 g kg 1 of feed (wet ration, four times as much in dry pellets). Wild crocodiles, and possibly carrier crocodiles on the farm, are believed to be the natural reservoir of infection. From the wild crocodiles the infection might be brought on to the farm by the use of river water in the rearing pens, while the spread from carrier animals on the farm might occur on the shoes of staff and the manager when moving from enclosure to enclosure or pen to pen.

Fig. 5.12. Chlamydial conjunctivitis with brinous exudate behind the third eyelid, Nile crocodile hatchling.

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Stress is suspected to play a role in triggering the outbreaks. The prevention of chlamydiosis must be based on stress prevention as well as on strict hygienic measures, such as the use of borehole or well water in the rearing section, as well as the disinfection of footwear when moving from section to section. It should be possible to prepare a diagnostic antigen which then could be used for screening crocodiles due to be sold or released, particularly Nile crocodiles from southern Africa.

Mycobacteriosis Mycobacteriosis is the disease caused by different species of Mycobacterium. Only the infection with the obligatory pathogens M. tuberculosis and M. bovis should be called tuberculosis. However, it is believed that these obligatory pathogens cannot infect crocodiles because of their very specic temperature requirements (Huchzermeyer and Huchzermeyer, 2000), although they can be adapted to growth at lower temperatures and thereby able to infect poikilothermic animals (Vogel, 1958). Only a few cases of mycobacterial infections in crocodilians have been reported, and these mostly from zoos and other collections: Mycobacterium marinum was isolated from four spectacled caimans, C. crocodilus, from London Zoo (Grifth, 1928); a case of renal tuberculosis was reported from a spectacled caiman without culture results (Zwart, 1964); a non-typeable strain of M. avium complex was isolated from a crocodile (Thoen and Schliesser, 1984); and acid-fast bacteria, which did not grow on culture media, were found associated with granulomatous lesions in a captive Chinese alligator (Blahak, 1998). Mycobacterium fortuitum was isolated from generalized granulomatous lesions of a captive spectacled caiman (Huchzermeyer and Huchzermeyer, 2000). The reported cases of farmed crocodiles are: a number of crocodilian cases with granulomatous lesions in lungs, trachea and intestines associated with mycobacteria, but without culture results (Youngprapakorn et al., 1994); generalized mycobacteriosis in 12

juvenile C. johnsoni, in which the agent was identied by a polymerase chain reaction (PCR) probe as M. ulcerans (Ariel et al., 1997b); granulomatous mycobacterial dermatitis in ve C. porosus, but without identication of the agent (Buenviaje et al., 1998b); and acid-fast bacteria found in a granulomatous lesion with giant cells in the foot of a farmed C. porosus hatchling (Turton et al., 1996). In addition, Huchzermeyer and Huchzermeyer (2000) reported several cases of generalized mycobacteriosis in farmed Nile crocodiles in South Africa caused by M. avium complex, while M. terrae, M. triviale and an atypical Mycobacterium were found to be environmental contaminants of granulomatous lesions caused by fungal infections. The infection usually takes place via the oralintestinal route and spreads from the intestine by septicaemia to all organ systems (see p. 228). The fat body appears to be particularly sensitive to mycobacterial infection, probably because of a lack of cells of the immune system (Fig. 5.13) (see also p. 262). The granulomatous lesions of crocodiles are non-specic and their presence does not indicate the presence of mycobacteria per se (Fig. 5.14). Mycobacteria have to be shown to be present by the use of a special stain (ZiehlNeelsen) (Fig. 5.15), by PCR or by culture. Note that the culture of mycobacteria from crocodiles can only be done in a specialized laboratory, as the media and procedures used for the culture of M. tuberculosis in medical pathology laboratories are not suitable for their isolation. The source of infection is either the food, e.g. pork infected with M. avium complex (Huchzermeyer and Huchzermeyer, 2000) and sh infected with M. fortuitum or M. marinum, or the environment. There is no treatment. For some cases the careful application of heat should be investigated, as M. ulcerans, for example, does not survive at 33C (Glynn, 1972). However, it is believed that high levels of vitamin C in the food may help to control the infection in the face of environmental contamination, as it does in sh (Chvez de Martnez and Richards, 1991). Strict hygiene comprising scrubbing and disinfection of the rearing pens with every water change, the boiling of raw meat

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Fig. 5.13. Mycobacterial steatothecitis in a case of generalized mycobacteriosis in a juvenile Nile crocodile.

Fig. 5.14. Mycobacterial granuloma in the fat body of a juvenile Nile crocodile (haematoxylin and eosin).

or sh from suspect sources and the provision of a stress-free environment are further prophylactic measures that can be taken.

Erysipelothrix infection Only one outbreak of Erysipelothrix insidiosa infection has been described, in a zoological exhibit in Florida, USA, where it caused gen-

eralized disease associated with mortality in 68-week-old spectacled caiman hatchlings, and dark-brown, crusty skin lesions, 24 cm in diameter, on the back of a very old American crocodile (estimated to be 100 years old). Treatment with penicillin in the feed and locally with an iodine spray led to the cessation of losses in the caimans and clinical improvement of the adult crocodile (Jasmin and Baucom, 1967).

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Fig. 5.15. Masses of mycobacteria in a granuloma in the spleen of a juvenile Nile crocodile (ZiehlNeelsen stain).

Clostridiosis Clostridial infections most likely are also precipitated by stress. It is only because of their apparent rarity that they are treated here under a separate heading. A Clostridium sp. was isolated from oedematous uid from four gharials that had oedematous swelling in all limbs and partial swelling of the abdomens. On palpation these swellings appeared to be painful (Misra et al., 1993). This description ts the common picture of polyarthritis following a septicaemia (see p. 228). A critically low water level in the pond housing the affected gharials (Misra et al., 1993) may have led to thermal stress and precipitated the disease. Clostridium septicum was isolated from a case of bacterial hepatitis/septicaemia from a farmed crocodile in Australia (Buenviaje et al., 1994). Clostridium limosum was isolated in Florida from the livers and kidneys of American alligators that died with symptoms of paralysis (Cato et al., 1970). Most likely the paralysis, in these cases, was due to polyarthritis, which often originates from stress-related septicaemias (p. 228). Clostridium spp. were reported to have been the second most important bacterial

isolates from 131 cases of hatchling alligator syndrome over 15 years on 25 farms in south-eastern USA (Barnett and Cardeilhac, 1995). A haemorrhagic enteritis associated with a clostridial infection is described in Chapter 7 (p. 257).

Dermatophilosis A Dermatophilus sp. was isolated from skin lesions referred to as brown spot in farmed American alligators in Louisiana. The lesions, in the form of a small discoloration between the abdominal scales, were reported to lower drastically the value of the hides (Bounds and Normand, 1991). However, Barnett and Cardeilhac (1998) failed to nd lamentous organisms in similar brown spot lesions in an alligator skin from Florida. Filamentous organisms have also been seen in histopathological preparations of skin lesions in Zimbabwe (Foggin, 1992b) and South Africa (the authors own cases) (Fig. 5.16), but they have never been isolated on culture media. The disease has been described in more detail from Australian crocodiles, where a Dermatophilus sp. was isolated from the lesions and the disease was transmitted

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Fig. 5.16. Dermatophilus-like organisms in a skin lesion in a juvenile Nile crocodile.

experimentally by the application of broth cultures to the skin of the trial crocodiles (Buenviaje et al., 1997, 1998a,b). The initial lesion consists of a lifting of the keratin accompanied by some accumulation of debris. This is followed by an indentation of the epidermis because of the continuous replacement of the necrotic cells and by hyperplasia of cells of the stratum basale. In the third stage the erosion of the epidermis results in ulceration with increased amounts of debris and the extension of the lamentous organisms into the subcutis (Buenviaje et al., 1998b). Broadly similar lesions are seen in a condition in Nile crocodiles called winter sores, which occurs in farmed crocodiles kept at suboptimal temperatures (Huchzermeyer, 1996c) (see pp. 236 and 241). Dermatophilus spp. are environmental organisms. Treatment of the infection can be tried by including tetracycline into the ration (1 g active substance per kg of food) for 10 days and by spraying the crocodiles themselves with a disinfectant such as F10 (Health and Hygiene, South Africa) or a 0.5% solution of copper sulphate or zinc sulphate (Van Tonder and Horner, 1994). The infection can be prevented by the application of very strict hygienic measures, such as regular thorough cleaning and disinfection of the rearing pens (see p. 113).

Non-specic septicaemias The non-specic septicaemias of crocodiles are caused by a large variety of bacteria of enteric or environmental origin, many of which are opportunistic rather than obligatory pathogens, mostly part of the normal intestinal ora (see p. 38), although the intestinal ora of farmed crocodiles may be modied by antibacterial treatments and the introduction of potential pathogens when feeding meat, particularly from farm mortalities. Septic wounds rarely lead to septicaemias (Huchzermeyer and Cooper, 2000) and this adds support to the hypothesis of the enteric origin of septicaemia in crocodiles. The infections usually are precipitated by stress (Jacobson, 1984) and may be exacerbated by suboptimal temperature regimes or by the inability of the affected crocodiles to thermoregulate effectively. As all these infections produce the same disease, there is no need to create a separate disease entity for each bacterium. There follows a list of bacteria isolated from cases of crocodilian septicaemias: Aeromonas hydrophila and A. shigelloides. In adult American alligators (Shotts et al., 1972; Gorden et al., 1979), in zoo crocodiles (Mayer and Frank, 1974), from the eyes of American alligators (Jacobson, 1984), in Nile crocodiles

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(Foggin, 1987, 1992a), in American alligator hatchlings (Peters and Cardeilhac, 1988; Barnett and Cardeilhac, 1995), in farm-reared C. porosus, C. johnsoni and Crocodylus novaeguineae (Ladds and Sims, 1990; Buenviaje et al., 1994). Bacillus sp. In American alligator hatchlings (Barnett and Cardeilhac, 1995). Campylobacter fetus subsp. jejuni. From a West African dwarf crocodile at Denver Zoological Gardens (Luechtefeld et al., 1981). Chromobacterium sp. In farmed New Guinea and Indo-Pacic crocodiles (Ladds and Sims, 1990). Citrobacter sp. and C. freundii. In American alligators (Novak and Seigel, 1986), in farmed Nile crocodiles (Foggin, 1992a), in American alligator hatchlings (Barnett and Cardeilhac, 1995). Corynebacterium sp. and C. pyogenes. In farmed Nile crocodiles (Foggin, 1992a), in American alligator hatchlings (Barnett and Cardeilhac, 1995). Edwardsiella sp. and E. tarda. In farmed Nile crocodiles (Foggin, 1992a), in American alligator hatchlings (Barnett and Cardeilhac, 1995) and from an adult female American alligator in a zoo (Wallace et al., 1966), in farmed C. porosus (Buenviaje et al., 1994; Hibberd et al., 1996). Enterobacter agglomerans. In American alligators (Novak and Seigel, 1986), in farmed Nile crocodiles (Foggin, 1992a), in farmed C. porosus (Hibberd et al., 1996). Escherichia coli. In an adult captive American alligator (Russell and Herman, 1970), in juvenile captive Crocodylus palustris (Sinha et al., 1988), in farmed Nile crocodiles (Foggin, 1992a). Klebsiella oxytoca and Klebsiella sp. In American alligators (Novak and Seigel, 1986) and in farmed crocodiles in Australia (Buenviaje et al., 1994). Morganella morgani. In a captive West African dwarf crocodile with subsequent arthritis (Heard et al., 1988), in American alligators (Novak and Seigel, 1986), in farmed Nile crocodiles (Foggin, 1992a), in farmed C. porosus (Hibberd et al., 1996). Pasteurella multocida. In captive American alligators that had been stoned

by trespassing persons (Mainster et al., 1972), in farmed Nile crocodiles (Mohan et al., 1994; Dziva and Mohan, 2000), in farmed C. porosus (Hibberd et al., 1996). Planococcus sp. In captive gharials (Misra et al., 1993). Proteus sp. In captive crocodiles (Mayer and Frank, 1974), in American alligators (Novak and Seigel, 1986), in a crocodile (Chakraborty et al., 1988). Providencia rettgeri. In farmed Nile crocodiles (Foggin, 1992a), in an adult female mugger from a zoo (Sinha et al., 1987), in farmed C. porosus (Buenviaje et al., 1994; Hibberd et al., 1996). Pseudomonas sp. and P. aeruginosa. In farmed Nile crocodiles (Foggin, 1992a), in farmed American alligator hatchlings (Barnett and Cardeilhac, 1995), in farmed spectacled caimans (Villafae et al., 1996), in farmed C. porosus (Hibberd et al., 1996). Pseudomonas putida in farmed C. porosus (Turton et al., 1996). Serratia sp., S. marcescens and S. liquefaciens. In American alligators (Novak and Seigel, 1986; Barnett and Cardeilhac, 1995) and in farmed crocodiles in Australia (Buenviaje et al., 1994). Staphylococcus sp. and S. aureus. In American alligators (Mainster et al., 1972), in a captive West African dwarf crocodile with subsequent septic arthritis (Heard et al., 1988), in American alligator hatchlings (Barnett and Cardeilhac, 1995). Streptococcus sp. In American alligator hatchlings (Barnett and Cardeilhac, 1995).

Clinical signs The course of the disease depends on the environmental temperature and the size of the affected crocodiles. It is fast in hatchlings kept at 3234C, but slow in juveniles at low temperatures, while it can take several months in adults. Hatchlings may die without showing any clinical signs. Juveniles and adults may refuse to feed, become lethargic and show a reddish discoloration of the ventral skin (Plate 9). In some chronic cases the affected animals develop white patches around the nostrils and eyes, as well as on

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the dorsal surface of body and limbs (Fig. 5.17) (see also p. 241). Even extreme emaciation is seen in some cases. In other instances the infection settles in the joints and other serous cavities, causing a polyarthritis or polyserositis (Plate 10). The crocodiles appear to be paralysed or rather unwilling or unable to move. The inammation of the joints may cause painful swelling of the legs (see p. 287). Pathology The ndings vary with the age of the animal and the course of the disease. In acute cases there may be no lesions at all. Diffuse or focal hepatitis, excess serous uid in body cavities, subcutaneous oedema, sometimes haemorrhagic, myocarditis and/or acute brinous epicarditis (Plate 11), as well as pneumonia, have been described (Mainster et al., 1972; Ladds and Sims, 1990; Foggin, 1992a). Splenomegaly is also a common feature (Huchzermeyer, 1994) (see p. 270). Treatment In advanced cases, the likelihood of a treatment being successful is minimal. If undertaken on a group basis, the treatment should

be based on the results of bacterial cultures and an antibiogram of the isolated agent, and should be administered via the food. Individual handling and injecting only adds to the stress that originally triggered the outbreak. At the same time, the environmental temperature should be adjusted to the optimal range and all stresses avoided. Only hatchlings can be caught and dosed or injected individually, as they appear to be stressed less by individual handling. Transferring sick animals to a hospital pen also causes further stress, and the necessity and consequences of such a move should be assessed beforehand. Prevention For the prevention of septicaemias it is necessary to maintain optimal temperature conditions and to keep handling and other stressful events to an absolute minimum. Since low temperatures do not allow the body to overcome a stress septicaemia, because of the inactivation of the immune system, crocodiles should not be handled, caught or transported in cold weather (winter) conditions, and during air transport the temperature should not be allowed to fall below 25C.

Fig. 5.17. White patches on the dorsal aspect of a juvenile Nile crocodile suffering from a chronic septicaemia.

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Fungal Infections
Opportunistic infections Most fungal infections are opportunistic. Many of the fungi involved in these infections are part of the normal intestinal ora and are excreted daily with the faeces into the water. They and the environmental fungi can thrive in the warm and humid conditions in the rearing house. However, they can also escape from the intestine and enter the blood circulation under severe stress (p. 278). This route of infection has been demonstrated in ostriches (Walker, 1912) and it is probably the most common origin of cases of generalized mycosis. Normally the fungi are inhibited in the intestine by the bacterial ora. If the latter is suppressed by prolonged antibacterial treatment, the fungi can multiply more freely (Silberman et al., 1977). Once a systemic infection has occurred, it depends on the suppression of the hosts immune system by cold or chronic stress to be able to fully establish itself. It is to be noted here that some of the fungi involved in these cases can multiply even under very cold conditions, exactly when the defenses of the host are immobilized by cold. Pathology The tissue reaction to fungal infections is granulomatous, and not exudative as it is in most localized bacterial infections. The granulomata are characterized by the presence of multinucleated giant cells. Fungal agents The following fungi have been isolated from crocodilians: Aspergillus avus. From farmed C. porosus (Hibberd et al., 1996) and from the skin of a farmed C. porosus (Buenviaje et al., 1998b). Aspergillus fumigatus. From skin lesions of farmed caimans (Troiano and Romn, 1996) and from the lungs of captive American alligators (Jasmin et al., 1968). Aspergillus niger. From farmed C. porosus (Buenviaje et al., 1994; Hibberd et al., 1996)

and from the skin of a farmed C. porosus (Buenviaje et al., 1998b). Aspergillus ustus. From the lungs of captive American alligators (Jasmin et al., 1968). Aspergillus versicolor. From farmed C. porosus (Hibberd et al., 1996). Beauveria bassiana. From the lungs of a captive American alligator (Fromtling et al., 1979a,b) and from the lungs of a captive Nile crocodile (Keymer, 1974). Candida albicans. From the oral cavity of a captive caiman (Debyser and Zwart, 1991). Candida parasilosis. From the skin of a farmed C. porosus (Buenviaje et al., 1998b). Candida sp. From the skin of two farmed C. porosus (Buenviaje et al., 1998b). Cephalosporium sp. From small white muscle lesions of a captive C. crocodilus (Debyser and Zwart, 1991) and from the lungs of captive juvenile caimans (Trevino, 1972). Cladosporium sp. From skin lesions of farmed caimans (Troiano and Romn, 1996). Curvularia lunata varaeria. From the skin of farmed C. porosus (Buenviaje et al., 1994). Fusarium moniliforme. From the lungs of a captive American alligator (Frelier et al., 1985). Fusarium solani. From internal organs of farmed C. porosus (Hibberd and Harrower, 1993; Buenviaje et al., 1994). Fusarium sp. From farmed C. porosus (Hibberd et al., 1996), from gingivae of a captive C. crocodilus fuscus (Kuttin et al., 1978) and from the skin of farmed C. porosus (Buenviaje et al., 1998b). Geotrichum candidum. From farmed C. porosus (Hibberd et al., 1996). Geotrichum sp. From farmed C. porosus (Hibberd et al., 1996). Metarhizium anisopliae. From the lungs of a captive crocodile (species not indicated) (Debyser and Zwart, 1991), from the lungs of a captive African dwarf crocodile (Keymer, 1974) and from the lungs of a captive American alligator (Jones, 1978). Mucor circinelloides. From the skin of a captive caiman (Debyser and Zwart, 1991) and from gastric ulcers of a captive crocodilian (Jones, 1978).

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Mucor sp. From the lungs of four captive crocodiles (Silberman et al., 1977). Paecilomyces farinosus. From the lungs of a captive American alligator (Jones, 1978). Paecilomyces sp. From farmed C. porosus (Hibberd et al., 1996). Penicillium lilacinum. From the lungs of ve captive crocodiles and alligators (Keymer, 1974). Penicillium oxalicum. From the skin of a farmed C. porosus (Buenviaje et al., 1994). Penicillium sp. From farmed C. porosus (Hibberd et al., 1996). Syncephalastrum sp. From the skin of two farmed C. porosus (Buenviaje et al., 1998b). Trichoderma sp. From the skin surface of a wild-caught American alligator (Foreyt et al., 1985). Trichophyton sp. From the skin of an American alligator (Jacobson, 1980, 1984). Trichosporon cutaneum. From the skin of one farmed C. porosus (Buenviaje et al., 1998b). Trichosporon sp. From tongue and gingivae of a captive Nile crocodile and a captive Caiman crocodilus fuscus (Kuttin et al., 1978).

ment is dangerous in this context. Regular changes of water, as well as scrubbing and disinfection of the pens, are essential measures. The crocodiles also have to be protected from prolonged exposure to suboptimal temperatures. Many fungi are psychrophilic, able to multiply at low temperatures. Simulating hibernation conditions for captive crocodiles kept in high-density situations is fraught with danger. Similarly, transporting crocodiles in winter regularly leads to high losses from generalized fungal infections. Crocodiles kept in a clean, hygienic and stress-free environment, at close to optimal temperatures at all times, are least likely to succumb to fungal infections.

Fungal dermatitis Fungal infections of the skin usually originate from infected wounds and abrasions. Stress, particularly thermal stress, may play an aggravating role. Debyser and Zwart (1991) report the isolation of Mucor circinelloides from the scales of a caiman. A supercial fungal dermatitis has been described by Foggin (1987), in which the dorsal skin appears dry and has a ne white coating, while in the mouth a more proliferative reaction can be seen. On histopathological examination, fungal hyphae and spores can be demonstrated in the supercial epidermis. Infections by Aspergillus, Penicillium and Curvularia spp. in C. porosus hatchlings caused a pale, gelatinous change in the affected skin of head, belly and tail, as well as between the scutes. The affected skin was sometimes ulcerated and sloughed easily (Buenviaje et al., 1994). Similar lesions were associated with Fusarium sp. and other fungi (Buenviaje et al., 1998b). Supercial growth of fungi on the skin may be facilitated by the deposition of nutrients on the skin from water which may be contaminated by food wastes. Histopathologically, the underlying skin is not affected. However, it appears that the dense fungal growth has a deleterious effect on the various functions of the skin, particularly in hatchlings. Foreyt et al. (1985) describe such a case in an American alligator. A similar

Treatment Systemic and respiratory infections are often diagnosed too late for treatment to be considered, while oral infections and dermatomycoses may be diagnosed early. In all cases of attempted treatment it is of utmost importance to rectify the triggering (environmental) circumstances, such as temperature and hygiene. The fungal load in the pens can be reduced by washing the surfaces with CuSO4 (1:1000) or a fungicidal disinfectant (F10, Health and Hygiene, South Africa). The actual topical treatment also depends on the sensitivity spectrum of the fungal isolate(s) from the particular case.

Prevention It is important to avoid excessive fungal build-up in the intestines as well as in the environment. Prolonged antibacterial treat-

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case was seen in intensively reared Nile crocodile hatchlings on a farm where very fat meat was fed. We called this condition greasy skin (Fig. 5.18). Spraying the pen and crocodiles with a detergent and hosing them down led to a speedy recovery (authors own unpublished ndings). Deep granulomatous lesions causing severe swellings are produced by fungal infection of skin abrasions and bite wounds on the feet of captive and farmed crocodiles (Figs 5.195.21). Jacobson (1984) describes these lesions as resembling bumblefoot in birds. However, these local infections in crocodiles do not provoke an exudative reaction (briscess) characteristic of bacterial infections (see p. 46), but are purely granulomatous. Ailing crocodiles often develop a fungal dermatitis at the tip of the tail (Figs 5.22 and 5.23).

Respiratory mycosis Fungal lesions in the lungs usually are of enteric origin and develop after severe stress or during prolonged exposure to cold (Frelier et al., 1985). A lung infection with Beauveria bassiana developed in a captive American alligator after exposure to cold temperatures (Fromtling et al., 1979a,b). Although the authors regarded this fungus

as an insect pathogen, it was found to be part of the normal intestinal ora of wild-caught African dwarf crocodiles (Huchzermeyer and Agnagna, 1994; Huchzermeyer et al., 2000) (see also Table 1.12). In the above case the fungal colonies spread to the serosal surface of the lung. Fungi isolated from lesions in the lungs include: Metarhizium anisopliae (Jones, 1978; Debyser and Zwart, 1991), Cephalosporium sp. (Trevino, 1972), Mucor sp. (Silberman et al., 1977), Aspergillus fumigatus and A. ustus (Jasmin et al., 1968), Beauveria bassiana, Metarhizium anisopliae and Penicillium lilacinum (Keymer, 1974), Paecilomyces farinosus (Jones, 1978), Fusarium moniliforme (Frelier et al., 1985) and Fusarium solani (Hibberd and Harrower, 1993). The lesions can either be small granulomata resembling tuberculous lesions (Figs 5.24 and 5.25) (Keymer, 1974), large granulomata, or conuent lesions with solidication of parts of the lung tissue (Fig. 5.26). Dilatation of the bronchi and the formation of emphysematous bullae have also been reported (Fig. 5.26) (Frelier et al., 1985) (see also p. 272). Treatment with systemic antifungals could be tried, but normally the condition is diagnosed post-mortem. The prevention is based on avoiding severe stress and prolonged exposure to cold.

Fig. 5.18. Nile crocodile hatchling covered in supercial fungal growth, greasy crocodile.

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Fig. 5.19. Small fungal granulomata between the toes of a juvenile Nile crocodile.

Fig. 5.20. Large fungal granuloma on the plantar surface of the left forelimb of a juvenile Nile crocodile.

Fig. 5.21. Large fungal granuloma on the dorsal aspect of the left hind limb of a juvenile Nile crocodile.

Gastrointestinal mycosis A case of gastric mycosis in a captive Nile crocodile was described by Kuttin et al. (1978). The crocodile also had gingival and tongue lesions (see below). Clearly circumscribed lesions of up to 3 cm diameter were present in the gastric mucosa, and fungal elements were

found in the lesions, supercially as well as penetrating deep into the muscular layer. A Trichosporon sp. was isolated from the oral lesions. Mucor circinelloides was isolated from large chronic gastric ulcers of a captive crocodilian (species not stated) (Jones, 1978). Intestinal lesions with fungal hyphae were found in generalized Fusarium solani

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Fig. 5.22. Dermatomycosis of the tail tip of a juvenile Nile crocodile.

Fig. 5.23. Fungal hyphae in a section of a mycotic skin lesion of a juvenile Nile crocodile.

Fig. 5.24. Small mycotic granulomata on the pleural surface of the lung of an adult Nile crocodile.

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Fig. 5.25. Small mycotic granulomata in the lung of an adult Nile crocodile.

Fig. 5.26. Conuent mycotic lesion at the caudal tip of the left lung and widespread emphysema in a juvenile Nile crocodile.

infections in farmed C. porosus in Australia (Hibberd and Harrower, 1993), as well as in crocodiles with Mucor sp. infections in addition to pulmonary lesions (Silberman et al., 1977). Gastric fungal lesions were found in an adult Nile crocodile as part of a generalized mycosis (Fig. 5.27) (authors own case).

Oral mycosis Mixed bacterial and fungal oral infections commonly occur in stressed and anorexic crocodiles (see p. 249). Candida albicans is frequently isolated from these lesions (Debyser and Zwart, 1991). Kuttin et al. (1978) found

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Fig. 5.27. Mycotic ulcers in the pyloric region of the stomach of an adult Nile crocodile with generalized mycosis.

Trichosporon sp. in tongue lesions of a captive Nile crocodile, and Fusarium sp. and Trichosporon sp. associated with gingival lesions in a captive Caiman crocodilus fuscus that had shared the same basin. The lesions can be conuent or well-circumscribed ulcers.

Generalized mycosis Generalized fungal infections usually are of enteric origin and commonly develop in stressed and anorexic animals, particularly in combination with prolonged exposure to suboptimal temperatures (Huchzermeyer, 1991b). An outbreak of generalized mycosis in juvenile farmed C. porosus was associated with abnormally low winter temperatures, and fungal lesions were found in livers and lungs (Buenviaje et al., 1994). Different organs and tissues may be affected. Debyser and Zwart (1991) report the isolation of Cephalosporium sp. from small, white muscle lesions in a C. crocodilus. In the case of pulmonary infection with Beauveria bassiana in a captive American alligator, there had been dissemination to liver and spleen (Fromtling et al., 1979a). How-

ever, more likely all the lesions originated from a fungaemia. Similarly, the cases of fungal infections in crocodiles and alligators described by Keymer (1974) were respiratory and systemic. Fusarium solani caused systemic infection in farmed C. porosus, affecting livers, lungs and intestines (Hibberd and Harrower, 1993). It is worth mentioning here that the inammatory response in reptiles is less specic than in mammals. In crocodiles, multinucleated giant cells are commonly present in granulomas and not limited to mycobacterial infections.

Parasitic Protozoa
Most parasitic protozoa, including some of the coccidia, are harmless commensals. Finding them is interesting from an ecological point of view. Parasites are an integral part of an ecosystem and of biodiversity. The extinction of a host causes the extinction of its parasites at the same time. Rescue and captive breeding of an endangered crocodile species may still not prevent the extinction of its specic parasites, particularly where the latter require intermediate hosts that are

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not present in the captive environment. The positive role of parasites in the evolution of the immune system, e.g. spleen size, has been demonstrated for birds (Morand and Poulin, 2000) and probably applies to all vertebrates.

species. However, it must be stated categorically that avian and mammalian coccidia from the animals fed to the crocodiles do not pose any threat. However, it is possible that Goussia sp. can be transmitted by shes used to feed the crocodiles. Life cycle

Coccidiosis Species of coccidia Coccidiosis is caused by several species of coccidia. A number of coccidian parasites of crocodiles have been described from faecal suspensions according to their oocyst morphology (see Tables 5.2 and 5.3), but in most cases without reference to any pathology, while, on the other hand, cases and severe outbreaks of coccidiosis, often involving internal organs as well as the intestine, have been described from many crocodilian species without denitive identication of the coccidian species involved (Table 5.4). Much further research is needed in this eld. Since sporozoites within the sporocysts are often the only stage found in cases of coccidiosis, it might be interesting to study the morphology of the sporozoites to determine which species are involved in causing outbreaks of disease. Some of the described species of Eimeria and Isospora may be very host specic, while others may be able to infect a wider range of
Table 5.2. The coccidia of crocodiles. Host Alligator mississippiensis A. mississippiensis Caiman Caiman yacare C. yacare Caiman latirostris Crocodylus acutus Crocodylus acutus C. niloticus C. niloticus C. niloticus Gavialis gangeticus Parasite Eimeria alligatori Eimeria hatcheri Eimeria pintoi Eimeria caimani Eimeria paraguayensis

The coccidia of the genera Eimeria and Isospora have a complex life cycle but do not require intermediate hosts. The oocysts are either excreted with the faeces and sporulate outside in the environment (exogenous sporulation) or sporulate while still in the intestine (endogenous sporulation). The sporulated oocysts of Eimeria contain four sporocysts with two sporozoites in each sporocyst (Figs 5.28 and 5.29), while those of Isospora contain two sporocysts with four sporozoites each. The sporozoites are liberated when the sporulated oocyst (or sporocyst) is ingested by a new host. However, in cases of endogenous sporulation, the sporozoites may be liberated within the same host and the development may continue without passing on to a new host. The sporozoites invade epithelial cells in the intestine, usually deep in the crypts, and there they develop into schizonts (Fig. 5.30). This process is called schizogony. The mature schizonts break up, at the same time destroying the host cell, and liberate merozoites, which, in turn, invade further

Pathology +++

References McAllister and Upton (1990) McAllister and Upton (1990) Carini (1933) Aquino-Shuster and Duszynski (1989) Aquino-Shuster and Duszynski (1989) Carini and Biocca (1940) Lainson (1968) Lainson (1968) Own material Thiroux (1916); Hoare (1932) Gardiner et al. (1986) Simond (1901b)

Isospora jacarei Eimeria crocodyli Isospora wilkei Eimeria sp. undescribed Eimeria sp. Goussia sp. Eimeria kermoganti

+++, Only species with which pathology was associated.

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Table 5.3. Characteristic features of the oocysts of crocodilian coccidia. Species Eimeria alligatori Eimeria caimani Eimeria crocodyli Eimeria hatcheri Eimeria kermoganti Eimeria parasuayeusis Eimeria pintoi Eimeria sp. of Crocodylus niloticus, undescribed Goussia sp. Isospora jacarei Isospora wilkei Size ( m) 25.3 20 1929 14.25 15.7 13.7 16.1 2022 23.6 34 33 22 13 12.6 20 13 15 22.8 33 Shape Ovoid Spheroid Spheroid Sub-spheroid Spherical Ellipsoid Ovoid Spheroid Spherical Sub-spherical Ovoid Shell Pitted Pitted Smooth Smooth Sporulation Exogenous

Micropyle Pitted

Exogenous Endogenous Endogenous Exogenous Endogenous Endogenous

Smooth Smooth

Table 5.4. Crocodilian species from which cases of coccidiosis have been reported. Host Caiman crocodilus Crocodylus niloticus Crocodylus novaeguineae Crocodylus palustris Crocodylus porosus Gavialis gangeticus G. gangeticus Intestinal x x x x x x Generalized x x x x x References 1 2, 3, 4, 5 6, 7 8 6, 7 8 9

1, Villafae et al. (1996); 2, Foggin (1987); 3, Foggin (1992a); 4, Foggin (1992b); 5, Obwolo and Zwart (1992); 6, Ladds and Sims (1990); 7, Ladds et al. (1995); 8, Jacobson (1984); 9, Griner (1983).

Fig. 5.28. Oocyst of an Eimeria sp. from a Nile crocodile; stained intestinal smear. Note the pitted surface of the oocyst shell.

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Fig. 5.29. Four sporulated sporocysts of the Nile crocodile Eimeria sp.; stained intestinal smear.

Fig. 5.30. Crocodile coccidia schizonts in a section of the intestinal mucosa.

epithelial cells. After several cycles of schizogony, the merozoites invading epithelial cells develop into macrogametocytes (female) and microgametocytes (male), and the latter liberate a large number of microgametes, which fertilize the female macrogametes. Subsequently these develop into oocysts, which can start a new cycle of infection (Fig. 5.31).

Sources of infection Infected crocodiles are the only source of the infection. This is of particular importance where the crocodile farm is situated in an area inhabited by wild crocodiles and where river or lake water is used on the crocodile farm. Adult breeding crocodiles can also carry the infection without being affected

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Fig. 5.31. Schematic drawing of the eimerian life cycle: 1, oocyst; 2, sporulated oocyst with four sporocysts containing two sporozoites each; 3, liberated sporocysts and sporozoites; 4, sporozoite infecting epithelial cell; 5, developing into a schizont; 6, schizont breaking up into merozoites, destroying the host cell and infecting further epithelial cells, either to form new schizonts (schizogony) or to begin gametogony; 7, merozoite infecting new cell; 8, to develop into a macrogametocyte (female) or into 9, a microgametocyte (male); 10, microgametocyte breaking up and liberating microgametes; 11, microgametes fertilizing the macrogamete, which develops into an oocyst 1.

themselves in any way. Attendants who have been working in the breeding enclosure can carry the oocysts or sporocysts on their feet or shoes into the rearing houses, and thus start an outbreak of coccidiosis in the hatchlings or juveniles. Feeding the intestines and internal organs of slaughtered crocodiles back to juvenile or even breeding crocodiles, a common practice on many crococile farms (see p. 128), may help to perpetuate the infection on the farm. It is possible that the Goussia sp., which appears to be responsible for outbreaks of generalized coccidiosis, uses shes as intermediate hosts, although it has been shown to be capable of direct transmission from crocodile to crocodile as well (Foggin, 1987).

Clinical signs Acute infections do not produce any clinical signs. However, as the infection progresses, the inammatory reaction to the presence of the coccidia, and possible secondary bacterial infections, produces masses of brinous exudate, which completely block the intestines. This causes the animal to become bloated rst and later to become lethargic. Some infected animals with blocked intestines may be able to survive for months, with a runted and emaciated appearance. Pathology In early cases there may only be a congestion of the intestinal mucosa with a serous

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exudate. Probably, the presence of secondary bacterial infections stimulates the prolic exudation of brin, once the intestinal bacteria have penetrated the epithelial barrier where the epithelial cells have been destroyed by the coccidia. Frequently this brinous exudate blocks the intestinal lumen. In early cases schizonts may be present in the epithelial cells of the crypts, while in advanced cases sporulated oocysts or liberated sporocysts may be found in the mucosa surrounded by intensive inammatory reaction and abundant brinous exudate (Fig. 5.32).

In some cases, some of the sporulated oocysts and sporocysts may be transported by the lymph to the general circulation and lodge in various internal organs (Fig. 5.33); however, in many cases without any noticeable inammatory response. Generalized coccidiosis In a particular form of coccidiosis, probably caused by Goussia sp., the developmental stages are seen to invade other internal organs, where they continue to multiply and cause a severe inammatory response

Fig. 5.32. Eimerian sporocysts with sporozoites deep in the intestinal mucosa of a juvenile Nile crocodile.

Fig. 5.33. Eimerian sporocysts with sporozoites in the pancreas of a wild-caught Osteolaemus tetraspis.

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(Gardiner et al., 1986; Foggin, 1987, 1992a,b). A similar case has been reported from a captive gharial (Griner, 1983). This generalized form of coccidiosis may even lead to the transovarial infection of crocodile embryos (Villafae et al., 1996) (see also p. 141). Therapy It is not possible to treat advanced cases of crocodilian coccidiosis because of the blockage of the intestine by the brinous exudate. However, as a herd treatment, sulphachloropyrazine (ESB3, Ciba Geigy) has been found to be particularly effective because of its simultaneous antibacterial activity (10 g of the water-soluble powder per 1 kg of food for 4 days, or dilute 1 g in 5 ml of water and dose by stomach tube at the rate of 0.2 ml per 100 g of body mass; Foggin, 1992a). Amprolium (Amprol 20% Logos Agvet; 2 g in 1 kg of food for 7 days) and Toltrazuril (Baycox, Bayer; 7 ml in 1 kg of food for 3 days) have also been found to be effective (Foggin, 1992a). Prevention The most important prophylactic measure consists in not allowing infected oocysts to enter the rearing section of the farm. Where the farm is situated close to waters inhabited by wild crocodiles, it is absolutely essential to avoid the use of surface water in the rearing pens. Note that chlorination of the water does not kill the oocysts. Separate shoes or rubber boots should be used for work in the breeding and rearing pens. Again, it must be stressed that disinfectant dips do not kill the oocysts that are carried on the shoes or boots. The continuous inclusion of a coccidiostat in the food does not seem to be practised anywhere, at least it has not been reported. However, on farms where outbreaks occur frequently, one could consider the prophylactic use of Toltrazuril in the food at monthly intervals. Foggin (1992a) recommends for such farms a prophylactic treatment with sulphachlorpyrazine (ESB3, Ciba Geigy), 10 g kg 1 food for 4 days, every 34 weeks.

Where generalized coccidiosis is a problem, one might also have to consider the possibility of food sh harbouring the parasite and introducing it into the farm.

Cryptosporidia Cryptosporidia are very small coccidian parasites of the intestinal epithelium. Their oocysts are approximately 4 5 m in size. They are mainly found in mammals and birds and are not very host specic. Because of their size, they are rarely found in direct faecal smears. Staining preparations with periodic acidSchiff (PAS) or Mayers haematoxylin improves chances of nding the oocysts (Lane and Mader, 1996). Histopathological examination of the intestinal mucosa is another way to detect cryptosporidial infections. At present there is no treatment for these infections. Cryptosporidia were found in the faeces of one out of nine captive Nile crocodiles in Egypt. The infection may have originated from infected attendants or from rats, which were fed to the crocodiles. The experimental infection of mice with cryptosporidia from the attendants, as well as from the crocodile, was successful (Siam et al., 1994). The infected crocodile did not show any clinical signs. This appears to be the rst and only report of cryptosporidia in crocodiles.

Hepatozoon (haemogregarines) A certain degree of confusion exists around these blood parasites, which originally were called haemogregarines, then split into the genera Haemogregarina and Hepatozoon, until all the crocodilian parasites of this group were nally transferred to the latter genus (Siddall, 1995; Smith, 1996). These belong to one of two groups of coccidian blood parasites of crocodilians, the other one belonging to the genus Progarnia (see p. 190), while Plasmodium spp., the true agents of malaria, have never been found in crocodiles. Members of the genus Hepatozoon are transmitted by arthropods in the case of the crocodilians, biting ies and mosquitoes,

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in which the sexual multiplication takes place (Chatton and Roubaud, 1913; Hoare, 1932; Pessa et al., 1972; Khan et al., 1980). Asexual schizonts are found in the liver of the infected crocodiles (Fig. 5.34), while gametocytes are found either in the red blood cells, typically folded over (Plate 12), or free in the blood as elongated vermiform bodies (Fig. 5.35). While developmental stages have also been found in leeches, it has not been possible to transmit the infection experimentally via these ectoparasites (Khan et al., 1980).

Confusion still surrounds the naming of individual Hepatozoon spp. of crocodiles. Some of the original descriptions gave insufcient detail and others were based on the assumption that each host species had its own haemogregarine parasite species. A list of the presently known named species is given in Table 5.5. However, a revision of the status of these species is required. The Hepatozoon spp. of crocodiles are able to sustain a high level of parasitaemia for many years, but do not appear to cause any harm to the host. However, it is possible that

Fig. 5.34. Hepatozoon sp. schizont in the liver of a wild-caught Osteolaemus tetraspis.

Fig. 5.35. Hepatozoon sp. free gametocyte in the blood of a wild-caught Osteolaemus tetraspis.

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Table 5.5. Hepatozoon spp. described from crocodiles. Note that the nomenclature is in need of revision. Alligator mississippiensis Caiman crocodilus C. latirostris Crocodilus frontatus Crocodylus cataphractus C. niloticus C. niloticus C. novaeguineae C. porosus Gavialis gangeticus Osteolaemus tetraspis
a

H. crocodilinorum H. brasiliensis H. caimani H. crocodilinorum H. sp. H. pettiti H. sheppardi H. sp. H. hankini H. hankini H. sp.

Brner (1901)a Di Primio (1925) Carini (1909) Brner (1901) Dutton et al. (1907) Thiroux (1910) Travassos Santos Dias (1952) Ladds and Sims (1990) Simond (1901a) Simond (1901a) Theiler (1930)

Redescribed by Khan et al. (1980).

chronically or terminally ill crocodiles may lose the ability to control the parasite, and this may lead to very high parasitaemias, which in turn could be falsely interpreted as cause of death.

Progarnia sp. Progarnia archosauriae (Haemosporina: Garniidae) is a parasite of red and white blood cells of C. crocodilus in northern Brazil (Lainson, 1995). Merogony takes place in lymphocytes and monocytes, less frequently in thrombocytes and even less frequently in immature and mature erythrocytes. The gamonts are found also in lymphocytes, monocytes and thrombocytes. The nuclear material of microgamonts is scattered diffusely, while the macrogamonts have a welldened nucleus and the characteristic blue-staining cytoplasm of female malarial parasites. The infection was found in very young, wild-caught animals. Nothing is known about the transmission of the parasite, presumably by biting insects, nor is anything known about a possible pathogenicity of the parasite.

manders and newts. It was found in a captive juvenile C. palustris (Parisi, 1910). Heavy trichomonad infections have been found in captive American alligators that died from colibacillosis (Russell and Herman, 1970) and in juvenile farmed C. crocodilus in a feeding trial (Avendao et al., 1992). While all these cases were associated with either mortality or poor performance, it remains unclear whether these parasites were the cause of death or poor performance, or were able to thrive in otherwise suppressed or stressed animals. Giardia sp. Giardias are binucleated agellates with an adhesive disk, which enables them to adhere to the intestinal epithelium. A Giardia sp., morphologically different from other known reptilian parasites of the same genus, was found repeatedly in farmed Nile crocodiles on several farms in South Africa, but did not appear to be associated with any pathology (authors own ndings). The trophozoites occur deep in the crypts of the intestinal mucosa and their cysts are excreted with the faeces (Figs 5.36 and 5.37). Leishmania (?) sp.

Intestinal agellates Trichomonas spp. Trichomonas prowazeki Alexeieff, 1909 has four anterior agellae and parasitizes sala-

Cases of severe giant cell enteritis in juvenile farmed C. porosus, usually under 1 year of age, with severely thickened walls of the upper intestine and associated with signs of chronic illness and runting, occurred in

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Fig. 5.36. Binucleated Giardia sp. trophozoite in a faecal smear from a farmed Nile crocodile.

Fig. 5.37. Giardia sp. trophozoites between the folds of the intestinal mucosa of a farmed Nile crocodile.

Australia and Papua New Guinea (Ladds et al., 1994). The giant cells contained intracytoplasmic bodies, which bore some resemblance to amastigotes of Leishmania spp. in mammalian histiocytes.

Trypanosomes The trypanosomes of crocodiles are harmless agellate blood parasites transmitted by

biting ies and possibly also mosquitoes. The life cycle of Trypanosoma grayi of the Nile crocodile in the tsetse y Glossina palpalis and its mode of transmission were studied by Hoare (1929, 1931). Trypanosomes are known from crocodiles and from caimans (Table 5.6). Normally the parasitaemia is so low that one rarely nds a trypanosome on a blood slide, even from infected crocodiles. However, one can improve the chances of nding the parasites by taking a larger blood

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Table 5.6. Crocodile species in which trypanosomes have been found. Host Crocodylus niloticus C. cataphractus Caiman crocodilus C. crocodilus
a Mean

Parasite T. grayi T. sp. T. cecili T. sp.

Length ( m) a 61.6 35 71.3 50.1

References Hoare (1928, 1929, 1931) Dutton et al. (1907) Lainson (1977) Nunes and Oshiro (1990)

length without agella.

sample, centrifuging it and making the smear from the buffy coat, the layer of white blood cells above the erythrocytes.

reptiles at Singapore Zoological Gardens, Blastocystis sp. was found in almost one-third of the species, including one C. porosus. All indications are that these parasites are harmless commensals (Teow et al., 1992).

Entamoeba sp. A single case of amoebic enteritis in a captive crocodile (no species given) has been reported, which happened in the course of an outbreak of amoebiasis in snakes and other reptiles in the affected collection (Ippen, 1965). This was associated with an exudative and necrotizing colitis (see also p. 257).

Metazoan Endoparasites
In contrast to the protozoa, the single-cell organisms of the preceding chapter, the metazoa are multicelled, with a variety of organs consisting of different tissues. The endoparasites in this group are the roundworms (nematodes) and the atworms, namely the trematodes (ukes) and cestodes (tapeworms).

Blastocystis sp. Blastocysts are intestinal parasites of uncertain taxonomic position of mammals, birds and reptiles. They have a typical cyst-like shape, 1015 m in diameter, with 24, or even more, nuclei (Fig. 5.38). In a survey of Ascaridoids The ascaridoid species A very large number of ascaridoid species have been described from crocodilians, demonstrating the rich and interesting biodiversity of crocodilian parasites. The species are listed below in alphabetical order, together with their hosts: Brevimulticaecum baylisi. Found in Alligator mississippiensis, C. crocodilus and Melanosuchus niger (Sprent, 1979b; Goldberg et al., 1991; Catto and Amato, 1994b). B. gibsoni. Found in M. niger (Sprent, 1979b). B. pintoi. Found in Caiman latirostris and C. crocodilus (Sprent, 1979b). B. stekhoveni. Found in M. niger and C. crocodilus (Sprent, 1979b; Goldberg et al., 1991; Catto and Amato, 1994b). B. tenuicolle. Found in A. mississippiensis (Hazen et al., 1978; Sprent, 1979b).

Fig. 5.38. Schematic drawing of a Blastocystis sp.

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Dujardinascaris angusae. Found in C. porosus (Sprent et al., 1998). D. antipini. Found in Crocodylus rhombifer (Groschaft and Barus, 1970). D. blairi. Found in C. johnsoni (Sprent et al., 1998). D. chabaudi. Found in C. johnsoni (Sprent, 1977). D. dujardini. Found in Crocodylus niloticus, Crocodylus cataphractus and C. porosus (?) in India (Bayliss, 1947; Sprent, 1977). D. gedoelsti. Found in C. niloticus (Sprent, 1977). D. harrisae. Found in C. porosus (?) and C. novaeguineae (Sprent et al., 1998). D. helicina. Found in Crocodylus acutus (Sprent, 1977). D. longispicula. Found in C. crocodilus (Sprent, 1977). D. madagascarensis. Found in C. niloticus and C. cataphractus (Sprent, 1977). D. mawsonae. Found in C. novaeguineae, C. porosus and C. johnsoni (?) (Sprent, 1977; Ladds and Sims, 1990; Sprent et al., 1998). D. paulista. Found in C. crocodilus (Sprent, 1977; Goldberg et al., 1991). D. philippinensis. Found in C. porosus (Machida et al., 1992; Sprent et al., 1998). D. petterae. Found in Osteolaemus tetraspis (Sprent et al., 1998). D. puylaerti. Found in C. niloticus (Sprent, 1977; Graber, 1981). D. salomonis. Found in C. porosus (Bayliss, 1947). D. tasmani. Found in C. niloticus (Ortlepp, 1932). D. taylorae. Found in C. porosus and C. novaeguineae (Sprent, 1977). D. waltonae. Found in A. mississippiensis (Sprent, 1977; Hazen et al., 1978; Cherry and Ager, 1982). D. westonae. Found in C. porosus (Sprent et al., 1998). D. woodlandi. Found in Gavialis gangeticus (Sprent, 1977). Gedoelstascaris australiensis. Found in C. johnsoni and C. porosus (Sprent, 1978a; Machida et al., 1992). G. vandenbrandeni. Found in C. niloticus and C. cataphractus (Sprent, 1978a). Goezia gavialidis. Found in G. gangeticus (Sprent, 1978b).

G. holmesi. Found in C. porosus (Sprent, 1978b). G. lacerticola. Found in A. mississippiensis (Deardorff and Overstreet, 1979). Hartwichia rousseloti. Found in C. niloticus and C. cataphractus (Graber, 1981; Sprent, 1983). Multicaecum agile. Found in C. niloticus, C. cataphractus, C. palustris, C. johnsoni, G. gangeticus and O. tetraspis (Sprent, 1979b; Graber, 1981). Ortleppascaris alata. Found in Crocodylus intermedius, C. crocodilus and probably M. niger (Sprent 1978a; Goldberg et al., 1991; Catto and Amato, 1994b). O. antipini. Found in A. mississippiensis and C. rhombifer (Sprent, 1978a). O. nigra. Found in C. niloticus, C. cataphractus and O. tetraspis (Sprent, 1978a; Graber, 1981). Terranova lanceolata (syn. braziliensis). Found in M. niger (Sprent, 1979a). T. crocodili. Found in C. niloticus, C. porosus, C. johnsoni (Sprent, 1983; Machida et al., 1992). Trispiculascaris assymmetrica. Found in C. niloticus (Sprent, 1983). T. trispiculascaris. Found in C. niloticus (Sprent, 1983). Typhlophorus lamellaris. Found in G. gangeticus (Sprent, 1983). T. spratti. Found in C. johnsoni (Sprent, 1999).

Life cycle Probably all ascaridoids of crocodiles require intermediate hosts, although this has been veried in only a few species. Larval forms taken from the amphibians Rana catesbiana, R. sphenocephala and Siren lacertina matured into adult examples of Brevimulticaecum tenuicolle when dosed to Alligator mississippiensis (Walton, 1936). It is likely that the life cycle of Dujardinascaris involves an encysted stage in sh, frogs or possibly other food animals. When swallowed by the crocodile, the third-stage larvae emerge in the stomach, where the fourth-stage larvae and adults also remain, usually attached to the stomach mucosa (Sprent, 1977). Dujardinascaris

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gedoelsti and D. dujardini were found in young farmed crocodiles in Zimbabwe after they had been fed with the lake sardine Limnothrissa miodon from Lake Kariba (Foggin, 1987, 1992a). Clinical signs and pathology Most ascaridoid infestations remain without clinical signs. Only in cases of very severe infestations will there be a certain degree of underperformance and runting (Foggin, 1992a). In subclinical cases the parasites remain in the stomach (Plate 13), but in severe infestations they may be found from the oesophagus to the cloaca. Often the ascaridoids are found associated with gastric ulcers, to which they attach (Figs 5.39 and 5.40) (Ortlepp, 1932; Ladds and Sims, 1990; Huchzermeyer and Agnagna, 1994; Ladds et al., 1995). However, it is not clear whether they can cause these ulcers or whether they only prefer to attach to mucosal lesions, once these exist. These mucosal lesions are surrounded by an intensive inammatory reaction (see also p. 25). Treatment Severe ascaridoid infestations can be treated by individual dosing with piperazine,

150200 mg kg 1 of body mass. For mass treatment, the vermifuge is given in the food: Fenbendazole (100 mg ml 1), 2 ml kg 1 of food, or Oxfendazole (22.6 mg ml 1), 5 ml kg 1 of food, both for 23 consecutive feeds (Foggin, 1992a). For better mixing, the drugs should be diluted in a small quantity of water. Prevention Crocodiles reared indoors and fed pelleted rations always are free of metazoan parasites. Therefore the best preventive measure against ascaridoid infestations is not to feed infected intermediate hosts to the crocodiles and not to allow live sh in the rearing ponds. Where the feeding of locally caught sh cannot be avoided, the larvae should be killed by freezing the sh for 72 h and thawing before feeding (Foggin, 1992a).

Capillarioids Crocodilocapillaria longiovata This is an apparently harmless parasite in the stomach of C. porosus, C. johnsoni and C. novaeguineae (Ladds and Sims, 1990; Ladds et al., 1995; Moravec and Spratt, 1998). The

Fig. 5.39. Stomach of a wild-caught African dwarf crocodile, with ulcers inhabited by ascaridoids.

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Fig. 5.40. Section of the gastric mucosa of a wild-caught African dwarf crocodile with ascaridoids penetrating deep into the mucosa and surrounded by a strong inammatory reaction.

larvae, as well as adults, were found coiled in the gastric glands without apparent tissue reactions (Ladds et al., 1995). Similar nematodes were found in the gastric glands of wild-caught O. tetraspis (Fig. 5.41) (authors own ndings). At our present state of knowledge preventative action and treatment do not appear to be necessary. Paratrichosoma spp. These capillarioid parasites are found in zigzagging burrows in the ventral skin of

crocodiles (Fig. 5.42). Two species are known so far: Paratrichosoma recurvum from C. acutus (Solger, 1877) and from Crocodylus morelettii (Moravec and Vargas-Vsquez, 1998), and P. crocodylus from C. novaeguineae (Ashford and Muller, 1978; Spratt, 1985) and C. porosus (Buenviaje et al., 1998). It is presumed that similar worm trails commonly found in wild-caught C. johnsoni are caused by the same parasite (Webb and Manolis, 1983). These zigzagging cutaneous trails are found in the skin of many crocodile species:

Fig. 5.41. Section of the gastric mucosa of a wild-caught African dwarf crocodile with capillarioid nematodes in the mucosal glands.

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Fig. 5.42. Zigzag trails caused by Paratrichosoma sp. in the belly skin of a farmed Nile crocodile (specimen brought from Malawi by P. Watson).

C. acutus (Solger, 1877); C. intermedius (King and Brazaitis, 1971); C. johnsoni (Webb and Manolis, 1983); C. moreletii (Moravec and VargasVsquez, 1998); C. niloticus (Foggin, 1987); C. novaeguineae (Ashford and Muller, 1978); C. palustris (Whitaker and Andrews, 1989); C. porosus (Buenviaje et al., 1998).

In view of the wide range of affected crocodile species and of their geographic distribution, it is possible that more hitherto undescribed Paratrichosoma spp. might exist (Moravec and Vargas-Vsquez, 1998). Little is known about the life cycle of these nematodes. The adult females are found burrowing in the cellular layer of the epidermis where the eggs are laid. With the constant formation of keratin, the old burrows containing the embryonating and embryonated eggs are slowly moved to the surface of the keratin layer, where, eventually, through abrasion, the eggs are voided into the environment (Elkan, 1974). On crocodile farms the parasites are found only if the crocodiles are kept in earth ponds, possibly indicating a requirement for the larvae to spend some time outside the host (Foggin, 1987).

It was assumed that after ingestion by another crocodile the larvae undergo their rst development in the stomach before migrating to the skin (Solger, 1877; Elkan, 1974). However, no signs of such migration have ever been described. Alternatively, it is possible that the freed larvae penetrate the skin directly from outside through the soft parts between the scales. In this they might perhaps be assisted by leeches (personal communication, C.M. Foggin, Harare, 1999). Ashford and Muller (1978) found fourthstage larvae already in the skin, and Moravec and Vargas-Vsquez (1998) found males and young females in deeper tissues of the skin, where fertilization is likely to take place. While not causing any inammatory reaction and pathology, the parasites cause considerable damage to the skin and its commercial value. However, no successful treatment of the lesions or elimination of the worms have yet been described. The benzimidazole drugs could be tried for treating the condition (personal communication, C.M. Foggin, Harare, 1999). If treatment is undertaken early enough and no re-infestation takes place, the skin should be able to recover. The most important preventive measure is not to rear the crocodiles in earth ponds.

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Trichinellae A Trichinella sp. morphologically identied as Trichinella spiralis was found in the meat of farmed crocodiles from 11 out of 17 farms in Zimbabwe, mainly in the pterygoid, mandibular and intercostal muscles (Fig. 5.43) (Foggin and Widdowson, 1996; Foggin et al., 1997). Larvae from affected crocodiles were infective to Zimbabwean domestic pigs (Mukaratirwa and Foggin, 1999) as well as to laboratory rats and baboons (Foggin et al., 1997). However, in another study, nine different Trichinella spp. isolates were found not to infect very young caimans (C. crocodilus) (Kapel et al., 1998). The infestation of the farmed crocodiles may have originated from infected venison or from scavenging rodents caught by the crocodiles. Treatment of infected crocodiles in the laboratory with albendazole, 50 mg kg 1 live mass, by oral dosing twice at 4-day intervals, removed the larvae from two crocodiles, while in the third crocodile only very few larvae could be detected in the pterygoid muscle after the treatment (Foggin et al., 1997). After freezing infected crocodile meat at 18C for 7 days it was no longer infective to rats (Foggin et al., 1997). The infestation of crocodiles can be prevented by feeding cooked meat or pelleted rations, in addition to strict rodent control. See Notes Added at Proof, p. 210.

Gnathostoma Third-stage larvae of Gnathostoma procyonis were found in the muscles of two American alligators in Louisiana. The denitive host of this hookworm is the racoon (Ash, 1962) (see p. 199). This nding may have some implications for the human consumption of alligator meat.

Filariae Parasite species Several species of lariae have been found in crocodiles: Micropleura vazii free in the abdominal cavity of C. crocodilus (Travassos, 1933; Troiano et al., 1998b; Goldberg et al., 1991). M. vivipara from G. gangeticus (von Linstow, 1906) and from C. niloticus (Foggin, 1987) although the latter author may not have been aware of Oswaldolaria versterae of the Nile crocodile (see below). Oswaldolaria bacillaris from the thorax wall of C. crocodilus (Molin, 1858 cited by Travassos, 1933; Prodhon and Bain, 1972). O. kanbaya from connective tissues and serous membranes of the body cavity of C. porosus (Manzanell, 1986).

Fig. 5.43. Trichinella sp. in the muscle of a farmed Nile crocodile (section sent from Zimbabwe by C.M. Foggin).

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O. medemi from Palaeosuchus trigonatus (Marinkelle, 1981). O. versterae from C. niloticus (Bain et al., 1982). Unidentied lariae have been found free in the abdominal cavity and under the pleura of the lung in C. novaeguineae (Ladds and Sims, 1990; Ladds et al., 1995). Life cycle The rst-stage larvae, microlariae, appear in the blood of the crocodilian host and are occasionally found in blood smears (Fig. 5.44) (Migone, 1916). They are ingested by a mosquito intermediate host with a blood meal. The morphology and development of the microlariae of O. bacillaris in the adipose tissue of the mosquito Anopheles stephensi have been described by Prodhon and Bain (1972). The third-stage larvae are retransmitted to a crocodilian host by a subsequent bite by the mosquito. Pathology No lesions have ever been found associated with the presence of adult lariae in crocodiles. Possibly the larvae are more pathogenic for the mosquito, when they invade its

optical lobes and ommatids (Prodhon and Bain, 1972).

Eustrongylids Immature specimens of Eustrongylides sp. have been found on the gastric serosa of C. porosus and C. novaeguineae (Ladds and Sims, 1990; Ladds et al., 1995) as well as in C. crocodilus, together with Contracaecum sp. (Goldberg et al., 1991). It is believed that both are parasites of piscivorous birds, with shes as intermediate hosts, and that the crocodiles are paratenic hosts only (Goldberg et al., 1991).

Rhabditids Large numbers of rhabditids (Caenorhabditis sp.) were found in bile ducts in the liver of a captive O. tetraspis, provoking an intensive inammatory reaction (Figs 5.45 and 5.46). Only a piece of liver in formalin had been submitted for examination (Huchzermeyer et al., 1993). Rhabditids are not very specialized, have a direct life cycle and can multiply rapidly in captive situations. It is possible that the unidentied small nematodes

Fig. 5.44. Microlaria in crocodile blood (photograph M.A. Peirce).

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Fig. 5.45. Rhabditid in a bile duct in the liver of a captive Osteolaemus tetraspis surrounded by an inammatory reaction.

Fig. 5.46. Rhabditid from the liver of a captive Afrian dwarf crocodile.

(5 mm) found in the inamed kidneys of a gharial hatchling by Maskey et al. (1998) were also rhabditids.

Hookworm There are only few reports of hookworms (Acanthocephala) in crocodilians. Polyacanthorhynchus rhopalorhynchus was found as part of the dominant helminth fauna parasitizing C. crocodilus yacare in the Brazilian Pantanal (Catto and Amato, 1994b), and

one juvenile specimen of Polymorphus mutabilis, a parasite of sh-eating birds, was found in 1 out of 21 examined Cuban crocodiles (Groschaft and Barus, 1970). One adult unidentied hookworm was found in a survey of parasites of wild-caught African dwarf crocodiles (authors own material). In a survey of reptiles in Louisiana, two out of four American alligators were found to have Gnathostoma procyonis larvae in their muscles (Ash, 1962). This is a parasite of raccoons in south-eastern USA. The alligators in

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this case were acting as second intermediary hosts (see also p. 197).

Trematodes found in the upper digestive tract (oral cavity, pharynx and oesophagus): Odhneriotrema incommodum in A. mississippiensis (Leigh, 1978). O. microcephala in C. crocodilus (Hughes et al., 1941; Catto and Amato, 1993a). Trematodes found in intestine and cloaca: Acanthostomum atae in C. porosus (Tubangui and Masilugan, 1936). A. caballeroi in C. crocodilus (Caballero, 1955). A. coronarium in A. mississippiensis (Hazen et al., 1978) and in C. acutus (Hughes et al., 1941). A. diploporum in A. mississippiensis (Hughes et al., 1941). A. elongatum in C. porosus (Tubangui and Masilugan, 1936). A. loossi in C. rhombifer (Groschaft and Barus, 1970; Brooks and Overstreet, 1977) and C. acutus (Prez Bentez et al., 1980). A. marajoarum in C. crocodilus (Hughes et al., 1941). A. pavidum in A. mississippiensis (Brooks and Overstreet, 1977). A. productum in C. niloticus (Hughes et al., 1941). A. quaesitum in C. johnsoni (Hughes et al., 1941; Brooks and Blair, 1978).

Trematodes Crocodiles harbour a rich and varied fauna of digenetic trematodes, which have been used to illustrate the co-evolution of the crocodiles with their parasites (Brooks, 1979; Brooks and OGrady, 1989). Monogenetic trematodes have been found as ectoparasites (see p. 209). The digenetic trematodes have two suckers with which they adhere to the intestinal wall (Fig. 5.47). The species The following hostparasite list is organized rst according to the site of the adult trematode in the host and secondarily in alphabetical order irrespective of trematode systematics, which should allow easy access to names and references. This list is certainly incomplete and not all quoted authors are necessarily the ones who rst discovered or described the parasites. Also, the nomenclature of some of the parasites may have changed in the course of ongoing revisions. As said before, the list is meant for easy access to references as a starting point for further research.

Fig. 5.47. Digenetic trematode from a Nile crocodile, the position of the two suckers indicated by arrows.

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A. scyphocephalum in C. crocodilus (Caballero, 1955). A. vicinum in C. niloticus (Hughes et al., 1941). Allechinostomum crocodili in C. niloticus and in Crocodylus siamensis (Hughes et al., 1941). Archaeodiplostomum acetabulatum in A. mississippiensis (Brooks et al., 1977; Hazen et al., 1978). Atrophocaecum acuti in C. rhombifer (Groschaft and Barus, 1970). A. americanum in C. rhombifer (Groschaft and Barus, 1970). A. caballeroi in C. rhombifer (Groschaft and Barus, 1970). Caimanicola marajoira in C. crocodilus (Catto and Amato, 1993a, 1994b). Capsulodiplostomum crocodilinum in C. palustris (Dwivedi, 1966). Crocodilicola caimanicola in C. latirostris (Dollfus, 1935). C. gavialis in G. gangeticus (Hughes et al., 1941). C. pseudostoma in A. mississippiensis (Byrd and Reiber, 1942; Brooks et al., 1977) and in Crocodylus sp. (Hughes et al., 1941). Cyatocotyle brasiliensis in C. crocodilus (Catto and Amato, 1994b). C. crocodili in C. johnsoni (Ladds and Sims, 1990) and C. porosus (Ladds et al., 1995). C. fraternae (fraterna?) in C. niloticus (Hughes et al., 1941; Bisseru, 1957). Cystodiplostomum hollyi in C. latirostris (Dubois, 1948) and C. crocodilus (Hughes et al., 1941; Catto and Amato, 1994a,b). Diplostome medusae in C. crocodilus (Hughes et al., 1941). Distoma pyxidatum in C. crocodilus (Hughes et al., 1941). Echinostoma jacaretinga in C. crocodilus (Hughes et al., 1941). Exotidendrium gharialii in G. gangeticus (Hughes et al., 1941). Harmotrema nicollii in G. gangeticus (Hughes et al., 1941). H. rudolphii in C. porosus (Tubangui and Masilugan, 1936). Herpetodiplostomum caimanicola in C. crocodilus (Hughes et al., 1941; Catto and Amato, 1994a,b), in C. latirostris (Hughes

et al., 1941) and in M. niger (Hughes et al., 1941). Mesodiplostomum gladiolum in C. crocodilus (Catto and Amato, 1994a) and in M. niger (Hughes et al., 1941). Neodiplostomum crocodilorum in C. porosus (Tubangui and Masilugan, 1936). N. gavialis in G. gangeticus (Narain, 1930). Neodiplostomum sp. in C. cataphractus (Hughes et al., 1941). Neoparadiplostomum kafuensis in C. niloticus (Bisseru, 1956). N. magnitesticulatum in C. niloticus (Bisseru, 1956). Neostrigea africana in C. niloticus (Bisseru, 1956). N. leiperi in C. niloticus (Bisseru, 1956). Nephrocephalus sessilis in C. niloticus (Hughes et al., 1941). Oistosomum caduceus in a Krokodil (Hughes et al., 1941). Pachypsolus constrictus in C. crocodilus (Hughes et al., 1941). P. sclerops in C. crocodilus (Catto and Amato, 1993a). Paradiplostomum abbreviatum in C. crocodilus (Hughes et al., 1941; Catto and Amato, 1994a,b) and in Crocodylus sp. (Hughes et al., 1941). Polycotyle ornata in A. mississippiensis (Byrd and Reiber, 1942; Brooks et al., 1977; Hazen et al., 1978). Proctocaecum dorsale in C. crocodilus (Catto and Amato, 1993a,b). Prolectithidiplostomum cavum in C. crocodilus (Hughes et al., 1941). P. constrictum in C. crocodilus (Brooks et al., 1977; Catto and Amato, 1994a,b). Prostrigea arcuata in C. niloticus (Bisseru, 1956). Proterodiplostomum breve in C. crocodilus (Catto and Amato, 1994a,b). P. globulare in C. crocodilus (Catto and Amato, 1994a,b). P. longum in C. crocodilus (Catto and Amato, 1993a, 1994a), in Crocodylus sp. (Hughes et al., 1941) and in M. niger (Hughes et al., 1941). P. medusae in C. crocodilus (Brooks et al., 1977; Catto and Amato, 1994a,b). P. tumidilum (tumidulum?) in C. crocodilus (Hughes et al., 1941; Catto and Amato, 1994a,b).

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Pseudocrocodilicola americana in A. mississippiensis (Byrd and Reiber, 1942; Hazen et al., 1978). P. georgiana in A. mississippiensis (Byrd and Reiber, 1942; Brooks et al., 1977). Pseudoneodiplostomum acetabulata in A. mississippiensis (Byrd and Reiber, 1942). P. bifurcatum in C. niloticus (Dubois, 1948) and O. tetraspis (Huchzermeyer and Agnagna, 1994) (Fig. 5.48). P. dollfusi in C. siamensis (Dubois, 1948). P. siamense in C. siamensis (Hughes et al., 1941). P. thomasi in C. cataphractus and O. tetraspis (Dubois, 1948). Pseudoneodiplostomum sp. in C. rhombifer (Groschaft and Barus, 1970). Pseudotelorchis caimanis in C. crocodilus (Catto and Amato, 1993b, 1994b). P. yacarei in C. crocodilus (Catto and Amato, 1993b, 1994b). Stephanoprora jacaretinga in C. crocodilus (Catto and Amato, 1994b). S. ornata in C. niloticus (Hughes et al., 1941). Timoniella absita in C. porosus (Blair et al., 1988). Trematodes found in the kidneys: Deurithitrema gingae in C. porosus (Blair, 1985). Deurithitrema sp. in C. porosus or C. novaeguineae (Ladds and Sims, 1990).

Exotidendrium sp. in Nile crocodiles (Foggin, 1992a). Plagiorchid ukes, previously undescribed, in C. novaeguineae (Ladds et al., 1995). Renivermis crocodyli in C. porosus (Blair et al., 1989). Trematodes found in blood vessels: Griphobilharzia amoena in C. johnsoni (Platt et al., 1991). Undetermined blood ukes in C. porosus and C. novaeguineae (Lads and Sims, 1990; Ladds et al., 1995). Trematodes found in the lungs: Undetermined trematodes and ova found in a granuloma in the lungs of a captive G. gangeticus (Griner, 1983). Life cycle All the above trematodes probably need two intermediate hosts, one invertebrate, such as small crustaceans or snails, and the second one a sh. However, the complete details have not been worked out for any of them. Pathogenicity and pathology There does not appear to be any pathology associated with infestations of intestinal

Fig. 5.48. Pseudoneodiplostomum bifurcatum from a wild-caught African Dwarf crocodile in the Congo Republic.

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ukes. While Prez Bentez et al. (1980) report high infestations with Acanthostomum loossi, associated with poor growth and high mortality, in farmed Cuban crocodiles, it is likely that other factors related to farming conditions and nutrition played a decisive role in the poor performance. No histopathological lesions were reported. Unless infested sh are fed, there is no possibility for high infestations to establish themselves in captive or farmed crocodiles. Leigh (1978) studied the modied hostparasite junction at the attachment site of Odhneriotrema incommodum in the oral mucosa. However, the nodule of brous connective tissue sloughs off after re-attachment of the parasite. Usually, the presence of blood and renal ukes was not accompanied by marked tissue reactions, although cases of pyelonephritis may have been caused by the latter (Ladds and Sims, 1990; Ladds et al., 1995). The unidentied trematode found in the lung of a captive crocodile (species not stated) was surrounded by a granulomatous reaction (Griner, 1983). Treatment and prophylaxis In the absence of severe pathogenicity, there should be no need for treatment. Captive and farmed crocodilians can be protected from infestation by not feeding fresh intermediate hosts, river sh from waters inhabited by wild crocodiles. If such sh are to be fed, they should be frozen thoroughly to kill larvae.

Larvae (plerocercoids) of the tapeworm Spirometra erinacei were found in the meat of farmed C. johnsoni slaughtered in the Northern Territory in Australia. The crocodiles had been reared in earth ponds. Since housing them in concrete pens the problem has disappeared (Melville, 1988; Millan et al., 1997b). A single cestode larva was found deep in the gastric muscularis of a New Guinea or Indo-Pacic crocodile (Ladds and Sims, 1990). A cestode larva was also found in a fragment of muscle attached to a piece of skin of an African dwarf crocodile during a 1996 survey of wild-caught crocodiles slaughtered at markets in the Congo Republic (Fig. 5.49) (authors own unpublished nding). Any such survey in the future should include the examination of muscle tissue. Cestode larvae are killed by freezing the meat at 10C for 24 h (Millan et al., 1997b).

Ectoparasites
Leeches Leeches are oligochaete annelid worms with suckers at both ends, allowing them a headover-tail motion while remaining attached to the surface with alternate suckers. They can also swim freely with a slow undulating motion. The parasitic leeches bite through the skin or mucosa at the attachment site on their host and suck blood. The species

Tapeworm cysts There are no published reports of adult tapeworms having been found in crocodiles, although Telford (1971) states that cestodes are commonly found in all groups of reptiles. Corrected later (Telford and Campbell, 1981), this fact remains unexplained, as tapeworms occur in sh, in other reptiles, in birds and in mammals. One reason suggested is the very low gastric pH of crocodiles, similar to that found in sharks, which also have no tapeworms (personal communication, M. Penrith, Pretoria, 2002).

The following species of leeches have been found on crocodiles; please note that the names quoted may have been revised in more recent taxonomic work (see Notes Added at Proof, p. 210): Haementeria lutzi fed experimentally on C. crocodilus (Pessa et al., 1972). Helobdella sp. on juvenile (<1 m total length) C. latirostris (personal communication, A. Larriera, Santa Fe, 2002). Hirudinaria manillensis, the buffalo leech, from larynx and lung of an IndoPacic crocodile (Jeffery et al., 1990). Philobdella gracilis from American alligators (Viosca, 1962).

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Fig. 5.49. Cestode larva in the nuchal muscle of a wild-caught African dwarf crocodile slaughtered at a market in the Congo Republic.

Placobdella multilineata from the American alligator (Forrester and Sawyer, 1974; Glassman et al., 1979; Khan et al., 1980; Cherry and Ager, 1982) and a captive Indo-Pacic crocodile in China (Yang and Davies, 1985). Placobdella papillifera from American alligators (Smith et al., 1976). Placobdelloides multistriatus from the Nile crocodile (Johansson, 1909; Moore, 1938; Oosthuizen, 1991), apparently a quite common parasite throughout Africa (Hippel, 1946; Flamand et al., 1992).

Pathogenicity The parasites attach to the oral mucosa, particularly the upper pits made by the crocodiles lower teeth (Smith et al., 1976) and to the skin: eyelids, external ears under the ear aps, ventral aspect of the neck, axillary region. Only Hirudinaria manillensis, the buffalo leech, was found in the respiratory tract (Jeffery et al., 1990), and may cause suffocation due to its size. At one stage it was believed that Placobdella multilineata was able to transmit haemogregarine infections (see p. 188). However, Khan et al. (1980) could not prove this mode of transmission. The buffalo leech

has been shown to be able to transmit rinderpest to water buffalos (Wharton, 1913). Similarly, leeches could play a role in the transmission of crocodile-specic viral and bacterial infections. American alligators infested with leeches had signicantly elevated eosinophil levels, which returned to normal within 6 weeks after the removal of the leeches (Glassman et al., 1979). On C. johnsoni, leeches were found congregating in skin punctures in the axillary region and, as there were no such dermal punctures in crocodiles without leeches, it was concluded that the leeches might be causing these dermal lesions (Webb and Manolis, 1983). Treatment and prevention Leeches are very sensitive to salinity (Telford and Campbell, 1981). Adding common salt (NaCl) to the water, probably 0.5%, should help to eliminate most leeches from an infested pond. Flamand et al. (1992) recommend dabbing attached leeches with alcohol or methylated spirits on a cotton swab. A variety of treatments for use against leeches on shes are given by Burreson (1995). Most of these are for short-time immersion, as used on sh farms, and none has actually been tried on crocodiles:

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NaCl 2.5% for 1 h; 200 g quicklime per 100 l for 5 s; a 0.2% solution of Lysol or 0.4% solution of Priasol for 515 s; a 0.005% solution of cupric chloride for 15 min; a 0.1% solution of Dylox 10 kills leech embryos but is toxic to sh (crocodiles?); Masoten 1 g in 4 m3 of water. All new acquisitions of captive crocodiles should be checked very carefully before releasing them into their new enclosures, and the same applies to terrapins (freshwater turtles), which frequently carry the same species of leeches, if they are to be kept with, or in close proximity to, the crocodiles. The introduction of Placobdella multilineata to China with the importation of American alligators (Yang and Davies, 1985) demonstrates this danger.

Ticks and mites Ticks Ticks are found occasionally on crocodiles, but no ticks habitually feed on crocodiles. Therefore they are unlikely to play a role in the transmission of infectious agents, as they do so commonly in birds and mammals. The following summarizes the few published reports of ticks found on crocodiles: Amblyomma dissimile on C. moreletii (Rainwater et al., 2001). Amblyomma (?) grossum on crocodiles (species not given) in Surinam (Neumann, 1899). Amblyomma sp. on C. johnsoni (Tucker, 1995). Amblyomma sp. on C. moreletii (Rainwater et al., 2001). Aponomma exornatum. Two male specimens found on a crocodile (species not given) in the Katanga Province of the Congo (now Democratic Republic of the Congo) (Schwetz, 1927a,b).

Biting insects Diptera Many biting ies and mosquitos may be feeding on crocodiles. However, few of these have been studied, mainly as vectors of other parasites: The mosquito Anopheles stephensi was found to act as intermediate host for Oswaldolaria bacillaris of C. crocodilus (Prodhon and Bain, 1972) (see p. 197). The mosquito Culex dolosus transmits Hepatozoon caimani (see p. 188) (Pessa et al., 1972). The tsetse y Glossina palpalis transmits Hepatozoon pettiti (see p. 188) as well as Trypanosoma grayi (see p. 191) (Chatton and Roubaud, 1913; Hoare, 1931, 1932).

Mites While mites are common ectoparasites on other reptiles, there are no published reports of mites on crocodiles.

Pentastomes Classication and biology Pentastomes are worm-like arthropods, a few millimetres to a few centimetres long, parasites of the respiratory system of reptiles, birds and mammals. An outline of the classication of the Pentastomida prepared by J. Riley of the University of Dundee, Scotland, is shown in Table 5.7. All crocodilian pentastomes have shes as intermediate hosts, and in their nal crocodilian hosts most inhabit the lungs, except Leiperia, which is found in the trachea, and Subtriquetra, which inhabits the nasal passages.

Other insects In failed experiments to transmit Hepatozoon caimani, 25 nymphs of the bug Triatoma infestans were placed into the caiman enclosure and two of them actually did feed on the caimans (Pessa et al., 1972). The bug transmits Chagas disease to people (Schoeld, 2001) but is unlikely to parasitize crocodilians in the wild.

206

Table 5.7. Outline of the classication of the phylum Pentastomida. Order Cephalobaenida Family Cephalobaenidae Genus Cephalobaena Raillietiella Reighardia Sebekia Aloa Leiperia Diesingia Sela Agema Subtriquetra Sambonia Elenia Waddycephalus Parasambonia Porocephalus Kiricephalus Armillifer Cubirea Gigliolella Linguatula No. of species 1 >35 2 12 5 2 1 1 1 3 (?) 4 2 10 2 8 5 7 2 1 6 Denitive host Snakes Snakes, lizards, amphisbaeniens, amphibians Marine birds Crocodilians (Chelonians) Crocodilians Crocodilians Chelonians Crocodilians Crocodilians Crocodilians Monitor lizards Monitor lizards Snakes Snakes Snakes Snakes Snakes Snakes Snakes Mammals Intermediate host ? Direct (?), insects, amphibians, lizards Direct (1 sp.) Fish (snakes, lizards?) Fish Fish ? Fish Fish Fish Direct (1 sp.) Amphibians, mammals Amphibians, reptiles, mammals Amphibians, reptiles, mammals Snakes, mammals Amphibians, lizards, mammals, snakes Mammals ? Mammals Direct (1 sp.), mammals

Porocephalida

Reighardiidae Sebekidae

Chapter 5

Subtriquetridae Sambonidae

Porocephalida

Armilliferidae

Linguatulidae

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Hostparasite list The following hostparasite list of crocodilian pentastomes was prepared by John Riley of the University of Dundee, Scotland.
ALLIGATOR MISSISSIPPIENSIS

Sebekia purdiae (Riley et al., 1990). Sela porosus (Riley, 1994).


CROCODYLUS PALUSTRIS

Sebekia mississippiensis (Overstreet et al., 1985).


CAIMAN CROCODILUS

Subtriquetra megacephala Sambon, 1922).


CROCODYLUS JOHNSONI

(Baird,

1853;

Aloa platycephala (Lohrmann, 1889; Giglioli, 1922). Sebekia trinitatis (Riley et al., 1990). Sebekia microhamus (Self and Rego, 1985). Subtriquetra subtriquetra (Diesing, 1835; Sambon, 1922).
CAIMAN LATIROSTRIS

L. australiensis. Sebekia johnstoni (Riley et al., 1990). S. multiannulata. S. purdiae.

CROCODYLUS NOVAEGUINEAE

Sebekia novaeguineae (Riley et al., 1990).


CROCODYLUS SIAMENSIS

A. platycephala.
MELANOSUCHUS NIGER

Sebekia jubini (Vaney and Sambon, 1910; Sambon, 1922) (species inquirenda).
OSTEOLAEMUS TETRASPIS

S. subtriquetra.
CROCODYLUS ACUTUS

Sebekia divestei (Giglioli, in Sambon, 1922).


CROCODYLUS NILOTICUS

S. okavangoensis. A. silvaepalustris. Aloa parva (Riley and Huchzermeyer, 1995b).


GAVIALIS GANGETICUS

Aloa nilotici (Riley and Huchzermeyer, 1995a). Leiperia cincinnalis (Sambon, 1922). Sebekia wedli (Giglioli, in Sambon, 1922). Sebekia cesarisi (Giglioli, in Sambon, 1922). Sebekia okavangoensis (Riley and Huchzermeyer, 1995a). Subtriquetra rileyi (Junker et al., 1998).
CROCODYLUS CATAPHRACTUS

Aloa indica (Hett, 1924) or Sebekia indica (Heymons, 1941).


PENTASTOMID SPECIES FROM UNDETERMINED

CROCODILE SPECIES

Agema silvaepalustris (Riley et al., 1997). S. okavangoensis.


CROCODYLUS POROSUS

Aloa simpsoni (Riley, 1994) from an unknown crocodile in Ghana. Sebekia acuminata (Travassos, 1924) from an unknown crocodile in Brazil. Sebekia samboni (Travassos, 1924) from an unknown crocodile in Brazil. Subtriquetra shipleyi (Hett, 1924) from the pharynx of an unknown Indian crocodile.

Aloa ginae (Giglioli, 1922). Aloa merki (Riley, 1994). Leiperia australiensis (Riley and Huchzermeyer, 1996). Sebekia multiannulata (Riley et al., 1990).

Pathogenicity and pathology In the lungs the parasites suck blood and thereby can cause infection and inammation. Sometimes large numbers of these para-

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sites can be found in crocodile lungs without any signs of tissue reaction (Fig. 5.50), while in other cases large lung abscesses are found associated with their presence. This is probably due to the state of nutrition and the general state of health of the host, as well as freedom from stress. In cases of stress septicaemia (see p. 228), the bacteria present in the blood can invade the lung tissue in the lesions caused by the pentastomes, and thus create the abscesses found associated with pentastome infestations. The frontal and subparietal glands of the pentastomes continuously secrete a surface membrane that covers vital areas of the hostparasite interface, and this is believed to protect the parasites from the hosts strong immune response (Riley et al., 1979). No lung lesions were found in 21 wildcaught O. tetraspis in the Congo Republic, which all had various numbers of pentastomes in their lungs (Huchzermeyer and Agnagna, 1994). Even high numbers of Aloa platycephala were not associated with any lung lesions in captive C. crocodilus nor in farmed caimans in Argentina (Troiano and Romn, 1996; Troiano et al., 1996b). In C. johnsoni and C. novaeguineae, the lesions associated with pentastomes consisted either of consolidation of the lungs or small, dark foci beneath the pleura (Ladds and Sims, 1990; Ladds et al., 1995). The

histopathological lesions consisted of extensive interstitial pneumonia, bronchiectasis and hyperplasia of the bronchiolar epithelium (Ladds and Sims, 1990). Wild-caught American alligators suffering from steatitis (see p. 219) appeared to have died from massive lung haemorrhage, with blood also in the stomach and intestines, apparently caused by the migration of the adult Sebekia oxycephala through the lung serosa (Deakins, 1971). Farmed American alligator hatchlings fed with live mosquito sh (Gambusia afnis) developed respiratory problems and began dying within 2 weeks. On post-mortem examination they had severe haemorrhages into the lungs, and large numbers of S. oxycephala were found in the lungs (Boyce et al., 1984). The fact that no pentastomes were found in wild American alligators under 40 cm length, and increasing numbers of the parasites with increasing length (Moreland et al., 1989), may be due to the initial prevalence of insectivorous behaviour in crocodilian hatchlings, with a gradual change-over to piscivory. It is possible that a slow build-up of parasite numbers with age allows the establishment of a balance between host and parasites (Moreland et al., 1989), but it could also be that sick and dying juvenile alligators are removed from the scene by cannibalism.

Fig. 5.50. Lung section of a Nile crocodile with a pentastome in an air passage. Note the absence of any tissue reaction.

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Diagnosis In severe infestations, pentastome eggs may be found in the hosts faeces. On post-mortem examination the parasites are found in the larger air passages of the lungs. In a fresh, dead crocodile, the suffocating pentastomes will come crawling out of cuts that have been made into the lung tissue (Figs 5.51 and 5.52). The high oxygen requirements and consequent air-seeking behaviour of pentastomes were described by Self and Kuntz (1967). Treatment Groups of captive crocodiles with known severe pentastome infestation may have to be treated. One problem here consists of the fact that few drugs have actually been tested on crocodiles, and that there may well be species differences in the sensitivity of crocodiles to various drugs. The antiparasitic Dectomax (doramectin 1%) has been tried out on Nile crocodiles, and the dose of 1 ml per 50 kg of body mass was found safe and effective (personal communication, C.M. Foggin, Harare, 2001), while ivermectin at effective doses is toxic (see pp. 89 and 225).

Prevention For the prevention of pentastome infestations, one has to bear in mind that sh are the intermediate hosts. Where sh from crocodile waters are to be fed to farmed or captive crocodiles, such sh should be frozen solid or boiled to kill the parasite larvae. Keeping live food sh in a crocodile breeding pond or exhibit should also be avoided, unless in such a case the crocodiles receive an antiparasitic treatment from time to time, say once a year. The prevention of stress is of major importance for allowing the crocodiles to overcome occasional bacterial infections caused by the pentastomes, and thereby preventing the formation of lung abscesses.

Monogenetic trematodes Monogenetic trematodes have been found within green slimy masses attached to the interdigital web and between the scales on the hind limbs of farmed crocodiles. The species was not determined (Youngprapakorn et al., 1994). Monogenetic

Fig. 5.51. Pentastomes crawling out of an incised lung of a Nile crocodile.

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Fig. 5.52. Pentastomes collected from the lungs of a Nile crocodile.

trematodes are common ectoparasites on shes, feeding on the mucus covering the piscine skin. It is possible that the specimens found in these cases were sh parasites nding a suitable medium in the slimy matter on the skin of the crocodiles, as the crocodiles epidermis normally would offer little attraction to these trematodes. The long agellae of the protozoa present in the same slime mass were most likely the polar laments of Myxobolus sp. which are protozoan ectoparasites of shes.

West Nile virus (page 163) An outbreak of West Nile virus infection has been diagnosed in american alligators in the USA (personal communication, E.R. Jacobson, Gainesville, 2003).

Trichinella (page 197) The crocodile parasite has been identied as Trichinella zimbabwensis by Pozio et al. (paper in press, International Journal of Parasitology) (personal communication, E. Pozio, Rome, 2003). Leeches (page 203) Placobdelloides stellapapillosa was found on Crocodylus porosus and Tomistoma schlegelii in Singapore Zoological Gardens (Govedich et al., 2002).

Notes Added at Proof


Embryonic cell lines (page 157) Several crocodilian broblast cell lines have been established recently at San Diego Zoo (personal communication, V.A. Lance, San Diego, 2002).

Chapter 6
Non-transmissible Diseases

Nutritional Diseases
In the wild, crocodiles eat a varied diet that supplies their nutritional needs but usually sustains a slow growth rate (see p. 98). Captive crocodiles frequently are given a monotonous diet, which may be decient in one or more essential constituents. Farmed crocodiles usually are pushed for a fast growth rate, and this can further accentuate potential imbalances in their articial nutrition. This may lead to deciencies of certain minerals and vitamins, and consequent disease and mortality.

Ca and P metabolism. Osteomalacia and brous osteodystrophy are the terms for the condition in young hatchlings where their bones fail to harden due to the lack of calcium. Rickets applies to malformations of the growing bone when due to the lack of vitamin D3 , the bones also fail to harden and become bent. Osteoporosis occurs in older juvenile and adults, where the already hardened bone structure becomes weakened by the withdrawal of calcium for metabolic needs. See Note Added at Proof, p. 239.

Causes Nutritional bone disease Synonyms Nutritional bone disease is an umbrella term that covers a range of related conditions and names, such as osteomalacia, rickets, secondary hyperparathyroidism, metabolic bone disease, brous osteodystrophy and osteoporosis. The umbrella term nutritional bone disease indicates the importance of nutritional factors in this condition. Metabolic bone disease shifts the emphasis to calcium (Ca) and phosphorus (P) metabolism. Secondary hyperparathyroidism places the accent on the role of the parathyroids in The most common cause of metabolic bone disease in young crocodiles is feeding with red meat without bone, or with an insufcient calcium supplement. This may be aggravated by a lack of vitamin D if the crocodiles are kept indoors. Vitamin D3 levels in the ration or in supplements can also deteriorate during prolonged storage under tropical conditions (Foggin, 1992a). However, an imbalance between calcium and phosphorus in any kind of ration can cause metabolic bone disease, although at a much slower rate. Malabsorption of calcium due to excessive phosphorus levels, or due to the presence of other minerals, can also cause the same condition.
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Symptoms In affected hatchlings the rst signs seen are a weakness and sluggishness. The animals become unable to walk on land, while they still can swim. Soon the contractions of the long back muscles cause distortions of the vertebral column, kyphoscoliosis (Fig. 6.1) (Cardeilhac, 1981; Tulasi Rao et al., 1984; Huchzermeyer, 1986; Matushima and Ramos, 1995; Troiano and Romn, 1996; Boede, 2000). On examination the bones are found to be pliable, particularly the jaw bones rubber jaws (Fig. 6.2) (Huchzermeyer, 1986; Foggin, 1992a). The teeth may fall out (Cardeilhac, 1981; Matushima and Ramos, 1995) or, more frequently, become diaphanous, like shards of glass glassy teeth (Huchzermeyer, 1986) and they may be pushed sideways into a horizontal position (Fig. 6.3) (Jacobson, 1984) (see also p. 247). The underlying hypocalcaemia may cause tremors or seizures, particularly when the crocodiles are being disturbed (Foggin, 1992a), and such seizures may lead to drowning, if they occur in the water. In older juveniles with less pliant vertebrae, these seizures may cause fractures of the spinal column (Figs 6.4 and 6.5), with consequent posterior paralysis (Foggin, 1987).

Osteoporosis in older juveniles is clinically associated with poor calcication of the teeth (see Fig. 6.9), but locomotion of the affected individuals does not appear to be adversely affected. Pathology On post-mortem examination, the bones of affected hatchlings are found to be very soft and they are easily cut with a scalpel. The curvature of the spine will be obvious (Fig. 6.6), as will be fractures of thoracic vertebrae (Figs 6.4 and 6.5), which may be associated with urine retention in the distended colon due to the posterior paralysis (Fig. 6.7). A longitudinal cut through the vertebral column may reveal compression of the spinal cord (Foggin, 1992a). Histopathology of the parathyroid glands may show proliferation and cystic degeneration (Fig. 6.8) (see also p. 275). Diaphanous teeth have also been observed in juvenile and even adult farmed Nile crocodiles (Fig. 6.9). Concomitant lesions on the long limb bones were found incidentally in slaughter crocodiles, and are clearly indicative of osteoporosis. The bones are very light and show marked areas of erosion, particularly close to the heads (Fig. 6.10). The

Fig. 6.1. Persisting kyphoskoliosis in a juvenile Nile crocodile after recovery from osteomalacia.

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Fig. 6.2. Rubber jaws and glassy teeth in a Nile crocodile hatchling with osteomalacia.

Fig. 6.3. Horizontal displacement of the teeth in a juvenile Nile crocodile that had suffered from osteomalacia.

condition occurs on many crocodile farms in South Africa (authors own cases) and has also been reported from Colombia (Blanco, 1997). Treatment and prevention For the treatment of nutritional bone disease, it is necessary to rectify the diagnosed deciency, usually that of calcium. If the affected hatchlings are too weak to feed by themselves, they can initially be dosed or injected

intraperitoneally (ip) with calcium borogluconate (250 mg ml 1), 1.5 ml kg 1 body mass. The corrected ration should contain additional calcium carbonate, dicalcium phosphate or sterilized bonemeal, to give a nal composition containing 1.52% calcium and a Ca:P ratio of 1.5:1. For individual crocodile hatchlings kept by hobbyists, a good source of calcium and phosphorus is found in the scrapings from a butchers saw, while calcium alone can be obtained from ground eggshells (hens eggs).

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Fig. 6.4. Fractured spine in a juvenile Nile crocodile which suffered from seizures due to acute hypocalcaemia.

Fig. 6.5. Fractured thoracic vertebra, indicated by a subpleural haemorrhage, in a juvenile Nile crocodile with acute hypocalcaemia.

Recovery takes place within a few days from the start of dosing with extra calcium. The hatchlings become active again and the bones harden. However, deformities of the

spinal column and of the jaws (teeth growing horizontally) will persist (Tulasi Rao et al., 1984; Huchzermeyer, 1986) (see also p. 247).

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Fig. 6.6. Deformed vertebral column in a Nile crocodile hatchling with osteomalacia.

Fig. 6.7. Urine-lled rectum in a juvenile Nile crocodile with fractured spine and posterior paralysis.

Parturition hypocalcaemia During the production of the eggshells, the female mobilizes calcium from her bones. If, for some reason, this process does not function perfectly, she may suffer from a hypocalcaemia, which in turn may interfere with the laying process, cause unnecessary straining

and a prolapse of the uterus. This condition may not necessarily be caused by a latent calcium deciency and could rather be precipitated by unusual weather conditions (see also p. 265). Treatment of the prolapse consists in immobilizing the female with Flaxedil or other muscle relaxant (see p. 70), cleaning

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Fig. 6.8. Parathyroid gland with cystic degeneration in a juvenile Nile crocodile hatchling suffering from nutritional bone disease.

Fig. 6.9. Diaphanous teeth due to insufcient calcium deposition in an adult farmed Nile crocodile.

the prolapsed uterus, pushing it back through the cloaca and securing it with a tobacco pouch suture, which is left in place for 23 days (see also p. 265).

Vitamin A deciency Vitamin deciencies occur when insufcient quantities of the various vitamins are present

in the bulk constituents of the ration, when insufcient levels of vitamins have been added to the ration, when the vitamins in the premix have deteriorated during prolonged storage on the farm or when the affected animals are eating very small quantities or nothing at all. In most of these cases more than one vitamin will be decient, leading to more complex symptoms. Hatchlings may be protected from vitamin deciencies by yolk-

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Fig. 6.10. Osteoporosis: erosions on the articular head of a leg bone of a juvenile Nile crocodile.

derived stores in their liver, until these stores have been used up (Ariel et al., 1997a). All vitamin deciencies can be treated by correcting the vitamin levels in the ration. In severe cases individual crocodiles can be injected with a specic vitamin preparation or a multivitamin suspension. Hatchlings can also be dosed with a nutrient uid enriched with the required vitamin(s) (see pp. 86 and 148). Vitamin A deciency has caused squamous metaplasia of the epithelium of the dorsal glands on the tongue of older crocodile hatchlings. Macroscopically these lesions appeared as pale to whitish nodular lesions (Foggin, 1987, 1992a; Ariel et al., 1997a). Squamous metaplasia of the epithelium of the kidney tubules was seen in the same hatchlings, together with an accumulation of uric acid crystals gout (see p. 230) (Foggin, 1987, 1992a; Ariel et al., 1997a). Squamous metaplasia has also been found in the conjunctivae (Foggin, 1987), although much of the conjunctivitis seen in Nile crocodile hatchlings may, in fact, be due to, or aggravated by, chlamydiosis (see p. 167). Grossly decient animals may develop

anasarca, generalized oedema (Foggin, 1987; Debyser and Zwart, 1991).

Thiamin deciency Thiamin (vitamin B1) is normally produced in sufcient quantities by the bacterial intestinal ora. Destruction of the intestinal ora by the unnecessary use of oral antibiotics may remove this source of vitamins (Thurman, 1990). Low quantities of thiamin are normally present in meats and sh, but the requirements for a fast growth rate may outstrip the naturally available vitamin supplies (Jubb, 1992). In addition, sh may contain a thiaminase that destroys the available thiamin. Repeated thawing and re-freezing of the minced meat may also destroy the thiamin present in the mince (Horner, 1988b; Jubb, 1992). Outbreaks of thiamin deciency have been reported in farmed Nile and IndoPacic crocodiles (Horner, 1988b; Jubb, 1992). In both cases frozen and thawed horse or donkey meat was fed to the hatchlings. The Nile crocodiles showed depression, lack

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of vocalization, paresis and quivering spasms, with the head and neck stretched out and lifted upwards (Horner, 1988b), while the Indo-Pacic hatchlings mainly showed a loss of righting reex and sluggishness, but with normal papillary reexes (Jubb, 1992). Both cases may have been complicated by a Ca:P imbalance due to the feeding of horse or donkey meat, particularly the case involving the Nile crocodiles, since Horner (1988b) also describes softened and degenerated lumbar vertebrae (see p. 211). In suspected cases of thiamin deciency Youngprapakorn et al. (1994) saw a paralysis and inward twisting of the lower forelimbs, with the hands lying palm up. The introduction of a more varied diet, and the supplementation with an appropriate vitamin premix, led to complete recovery in all cases.

Vitamin C deciency Crocodiles, like most animals, can synthesize their own vitamin C, ascorbic acid, and therefore symptoms of classical scurvy-like vitamin C deciency are unlikely to be seen. However, under certain circumstances, such as stress and infection, the vitamin C requirements may exceed the bodys own produc-

tion. As a powerful scavenger of oxygen radicals, vitamin C, together with vitamin E, supports the function of leucocytes in the respiratory bursts during phagocytosis (the destruction of invading bacteria) (Bendich, 1990; Boxer, 1990). A direct protective action of vitamin C against specic bacterial and protozoan infections has been demonstrated in several sh species (Li and Lovell, 1985; Wahli et al., 1986; Chvez de Martnez and Richards, 1991) as well as in poultry (Gross, 1992). Ascorbic acid also supports the action of nitric oxide in vascular endothelial cells and thereby helps to protect vascular integrity (Heller et al., 1999). Furthermore, ascorbic acid plays a role in the synthesis of corticosteroids in the adrenal glands, and stress can lead to the depletion of ascorbic acid in the adrenals (Perek and Eckstein, 1959). Consequently, supplementary vitamin C can help to protect the animals against the consequences of stress. Cases of ulcerative gingivitis, with bacterial and fungal complications, in farmed juvenile Nile crocodiles (Fig. 6.11), which were refractory to antibacterial treatment, responded rapidly to intramuscular (im) injections with vitamin C ( 25 mg per kg live mass, repeated after 48 h) and/or continuous feeding of vitamin C in the ration at

Fig. 6.11. Nile crocodile hatchling with ulcerative gingivitis.

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1 g kg 1 of feed (Huchzermeyer and Huchzermeyer, 2001) (see also p. 249). The supplementation of crocodile rations with ascorbic acid at the above level is now a routine recommendation in South Africa.

Vitamin K deciency Vitamin K plays a role in blood coagulation and a deciency may cause prolonged bleeding from minor wounds or when replacing teeth (Thurman, 1990). The vitamin is normally taken in with the intestinal contents of the prey. An exclusively meat diet, particularly horse or donkey, could lead to a vitamin K deciency, and in all cases of severe internal or external haemorrhage, the possibility of such a deciency should be taken into account. However, rodenticide (warfarin) poisoning should also be considered (see p. 224).

Vitamin E deciency In addition to its role in gonadal development and function, and to its vitamin C-like oxygen radical scavenging function in the immune response (see p. 218), vitamin E as antioxidant also protects against the toxic effects of rancid fats, particularly sh oils. In some of these functions vitamin E is supported by selenium. Steatitis fat necrosis Fat necrosis is due primarily to the toxic action of rancid sh oils, which are often consumed by farmed crocodiles fed sh which is not quite fresh any more, such as market left-overs. In the crocodile this causes the fatty tissue to die and to undergo saponication, to harden. The saponied fat is regarded by the body as foreign substance and consequently elicits an inammatory reaction steatitis. The hardened fat reduces the motility of the animal. Saponication of the large intermuscular fat deposits in the tail may render the tail entirely immobile and the affected crocodile unable to swim, while the hardening of abdominal fat may

interfere with the motility of the intestines. Also, the saponied fat is no longer available as source of energy. There may be acute mortality, but in other cases the affected crocodiles may be able to survive and continue growing until their slaughter. The inammation and necrosis of all fat deposits is called pansteatitis. Cases of fat necrosis have been reported from American alligators (Wallach and Hoessle, 1968; Wallach, 1970; Larsen et al., 1983), Caiman crocodilus (Wallach and Hoessle, 1968; Frye and Schelling, 1973), Nile crocodiles (Foggin, 1992a,b), a crocodile (unspecied) in Irian Jaya (Ladds et al., 1995) and Cuban crocodiles (Moliner et al., 2000b). Clinically, the affected crocodiles may appear sluggish. The strips of hardened fat in the tail can be palpated. On post-mortem examination the hardened yellow or brownish fat surrounded by inamed tissue cannot be overlooked (Plates 14 and 15, and Fig. 6.12). If fat necrosis is found at slaughter, the whole carcases should be condemned. There is no effective treatment to reverse the saponication of the fat. High doses of vitamin E may help to arrest the process. As prevention, only fresh sh should be given, if sh is the main source of nutrition for the captive or farmed crocodiles. Fatty shes should be avoided. In addition, a supplement containing adequate levels of vitamin E should be mixed into the ration (see p. 99). White muscle disease Inadequate amounts of vitamin E and selenium in the diet may cause certain muscles to degenerate Zenkers degeneration. The muscles take on a white appearance white muscle disease and are unable to contract, causing the affected animal to be paralysed. Zenkers degeneration (Fig. 6.13) was found in a group of 1-year-old farmed Nile crocodiles in Botswana, which were unable to walk and presented with swollen upper arms and thighs. However, it was not possible to pinpoint the cause of the deciency, nor did injections with vitamin E and selenium lead to a rapid recovery (authors own unpublished ndings). However, in a limited trial in Zimbabwe, Nile crocodile hatchlings

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Fig. 6.12. Fat body of a juvenile Nile crocodile with pansteatitis.

Fig. 6.13. Section of leg muscle of a farmed Nile crocodile with white muscle disease, Zenkers degeneration.

injected im with a selenium and vitamin E preparation gained more weight during the 2-month observation period than the untreated controls (Foggin, 1987). Zenkers degeneration may have been the cause of muscular calcication described by Youngprapakorn et al. (1994). Degeneration

of the heart muscle was seen in one captive juvenile gharial and thought to have been caused by feeding sh that were not entirely fresh (Maskey et al., 1998). White muscle disease, together with pansteatitis, occurred in farmed Cuban crocodiles (Moliner et al., 2000b).

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Cloacal ulcerations Linear ulcerations of the cloaca, lled with yellow keratinized debris, encountered in crocodilians may also be caused by vitamin E deciency (Wallach, 1971). Poor reproductive performance Fish-fed female alligators had signicantly lower plasma vitamin E levels than nutriafed and wild female alligators, and this may be partially responsible for the lower rate of fertility of the eggs of the sh-fed females, and generally for reproductive failure in shfed captive crocodiles (Lance et al., 1983).

Nutritional hypoproteinaemia Matushima and Ramos (1995) describe a nutritional hypoproteinaemia caused by a low protein diet in farmed caimans, but did not specify the ingredients of such a diet. Clinically they saw paleness, muscular weakness, depression and anorexia, and, on post-mortem, watery blood, generalized oedema, hydropericardium, ascites and diminished spleen size. In cases of prolonged anaemia they also saw necrosis of the liver. All these symptoms and lesions are commonly found in runting (see p. 234), which does occur in spite of adequate rations being offered, rather being due to insufcient nutrient intake. In general it is quite unlikely that crocodilians could be given a ration decient in protein.

stances, but also much more insidiously through the slow accumulation of low levels of agricultural and industrial pollutants from upstream human activities. Being in an aquatic environment and at the top of the food chain makes crocodiles particularly vulnerable to the effects of pollution. Unfortunately, cases of mortality in wild crocodiles often go unnoticed for long times, and it is usually not easy to collect adequate specimens. The chemical analysis required for the investigation of such cases needs sophisticated laboratory facilities, which are lacking in many tropical countries. The analyses themselves are costly and funds are scarce anywhere in the crocodile world. However, in a well-planned and funded programme, crocodilian populations can be used to monitor levels of pollution (Cardeilhac et al., 1999a,b). Some of the reports below are rather about levels of contaminants found, sometimes multiple, than actual cases of toxicity.

Heavy metals Heavy metals may be naturally present in the environment, or may originate from industrial activities. Both mercury and lead have a tendency to bio-accumulate. The tolerance of crocodilians to lead and mercury may be very high. Only one case has been documented of an adult American alligator (total length 3.92 m), life-long resident in a contaminated reservoir, which was found dead and emaciated and had wet-mass mercury levels of 3.48 g g 1 in the muscle, 33.55 g g 1 in the kidney and 158.85 g g 1 in the liver (Brisbin et al., 1998). Levels of various elements found in the tissues of wild American alligators and Nile crocodiles are presented in Tables 6.1 and 6.2, and mercury levels in tissues of American alligators in Tables 6.3 and 6.4. Mercury was also found in the eggs of Morelets crocodiles in Belize (Rainwater et al., 1997). Mercury levels in the meat are also of concern from a public health point of view (Hord et al., 1990; Brazaitis et al., 1996; Brisbin et al., 1998). From the tissue levels in Tables 6.3 and 6.4 it becomes clear that,

Zinc deciency Supercial erosion of the skin and decolorization often are seen in chronically ailing juvenile crocodiles (see p. 241). Youngprapakorn et al. (1994) suspect these cases to be caused by combined zinc and biotin deciencies.

Poisoning
Poisoning occurs not only through the deliberate or accidental ingestion of toxic sub-

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Table 6.1. Ranges of mean metal levels in alligator meat (Delaney et al., 1988), eggs (Heinz et al., 1991), embryos (Van Heeckeren et al., 1988) and liver, fat and tail muscle (Burger et al., 2000) from different lakes in Florida, USA, in g g 1 wet basis. Metal Aluminium Arsenic Beryllium Cadmium Chromium Copper Iron Lead Manganese Mercury Molybdenum Nickel Selenium Thallium Vanadium Zinc Tin Meat Eggs 1.32.0 BD BD BD 0.080.09 0.320.78 1113 BD0.22 0.140.15 BD BD 0.300.37 BD BD 5.67.6 Embryos BD 0.041 BD 0.290.53 8.7616.42 BD 0.127 0.133 0.0351 0.0738 0.113 0.0241 0.078 0.252 Liver Fat Tail muscle

0.010.06 0.030.11 0.286.03 4.5622.76 0.040.12 0.040.61

0.00986 1.380 0.108

0.0196 0.369 0.010

0.0267 0.802 0.057

1.1812.76 0.429 0.256 0.187

14.2036.0

0.231

0.165

0.726

BD, below detection. Note that in their paper Burger et al. (2000) mistakenly equate p.p.b. with g g 1.

Table 6.2. Ranges of mean metal levels in g g 1 in frozen Nile crocodile tissues from three different rivers in the Kruger National Park, South Africa (Swanepoel et al., 2000). Metal Al Cu Cr Fe Mn Ni Pb Sr Zn Muscle 73.5367.8 7.912.6 9.890.5 156.0615.0 0.117.8 9.124.9 BD3.7 6.726.7 39.4109.7 Liver 175.2487.6 23.230.6 5.169.0 690.812,851.3 0.115.5 7.323.0 019.85 6.624.4 61.5122.5 Kidney 40.8360.6 3.513.9 0.782.0 131.3520.0 0.1217.6 BD28.9 BD9.7 8.032.5 54.294.4 Fat 55.6367.6 6.17.6 14.6105.4 188.1297.7 0.118.7 12.831.2 BD8.5 6.923.2 7.611.2

BD, below detection.

Table 6.3. Ranges of mean mercury levels in tissues of American alligators from different sites, in g g dry mass. Tissue Tail scute Claw Muscle Liver Kidney Yanochko et al. (1997) 5.126.33 4.085.69 17.7342.15 35.0038.46 Jagoe et al. (1998) 0.295.83 1.672.69 0.805.57 4.3041.03 4.8236.42 Hord et al. (1990)

0.462.88

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Table 6.4. Mean tissue mercury levels of American alligators, wild from contaminated and uncontaminated habitats and farm-raised (in g g 1 wet mass) (Heaton-Jones et al., 1997). Tissue Liver Kidney Tail muscle Brain Leg scales NonEverglades Everglades 39.99 25.85 2.61 1.37 0.82 2.52 1.58 0.33 0.16 0.35 Farmraised 0.10 0.09 0.10 0.08 0.08

Table 6.5. Mean values of metals found in the shells and soft contents of Crocodylus acutus eggs ( g g 1 dry mass) (Stoneburner and Kushlan, 1984). Metal Aluminium Cadmium Cobalt Chromium Copper Lead Mercury Molybdenum Nickel Strontium Shell 52.36 1.36 1.70 20.46 17.17 16.42 0.21 25.43 22.04 529.50 Soft contents 10.86 0.13 1.12 2.64 6.21 3.35 0.66 2.37 2.35 45.65

contrary to feathers and hair, mercury does not appear to be concentrating in crocodile scales. Accordingly, there is no possibility of non-invasive sampling. Mercury may be present normally in aquatic environments or may originate from agricultural, mining and gold extracting (amalgamate process) activities (Brazaitis et al., 1996). Lead levels in the blood of two clinically normal adult female false gharials and a Cuban crocodile at New York Zoological Park were 147, 178 and 247 g dl 1, respectively. The crocodiles had been fed with urban feral pigeons (Cook et al., 1988, 1989). The pollution of the urban environment with lead is mainly due to the exhaust fumes from motor vehicles using leaded fuels. An elevated serum zinc level of 45.3 g ml 1 was found in a Cuban crocodile that had swallowed a number of coins. After removal of the coins, with the help of a colonobrescope tted with retrieval forceps, the animal was treated with CaEDTA at 40 mg kg 1 live mass every second day, six treatments in all. Thirty-nine days later, the zinc level had dropped to 4.88 g ml 1 (Cook et al., 1989). Nothing is known of the toxicity of other metals in crocodiles. Metal levels found in the shells and soft contents of eggs of Crocodylus acutus by Stoneburner and Kushlan (1984) are presented in Table 6.5.

sist in the environment for a very long time. They have a tendency to bio-accumulate and therefore the crocodile, at the top of the food chain, is particularly vulnerable. These contaminants have been found in crocodilian samples from various populations in Africa, as well as in North and Central America (Hall et al., 1979; Wessels et al., 1980; Delaney et al., 1988; Phelps et al., 1989; Heinz et al., 1991; Skaare et al., 1991; Cobb et al., 1997; Rainwater et al., 1997). Fatty sh, in particular, have been blamed for being able to carry high loads of pesticides (Joanen and McNease, 1979). Levels of polychlorinated biphenyls in the chorioallantoic membranes of neonatal American alligator hatchlings were signicantly correlated with concentrations in fat and yolk (Bargar et al., 1999). Accumulation of these compounds in the tissues may render the meat from such crocodiles unsuitable for human consumption. After baiting with 105 bait (Mirex) against re ants, Solenopsis spp., residues were found in tissues of American alligators. Two years later the levels were signicantly reduced (Wheeler et al., 1977). While gross direct poisoning of crocodiles has not been described, a most insidious effect of some of these compounds was discovered more recently: Endocrine disruption Some of these compounds can mimic sex hormones and, at very low levels, can affect

Pesticides Some pesticides and similar industrial organic compounds are very stable, or break down into stable compounds which can per-

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the sex ratio of hatchlings, interfere with the development of sexual organs and generally affect the reproductive success of a crocodile population in a contaminated environment. This effect has been documented for several lakes in Florida, USA (Woodward et al., 1993; Guillette et al., 1994, 1995a, 1996, 1999; Vonier et al., 1996; Crain et al., 1997, 1998; Cardeilhac et al., 1998; Crews and Ross, 1998; Matter et al., 1998). The most worrying fact here is that there is no safe level, that no threshold dose exists, as the mimicked substance already is present and the slightest addition to it is able to affect the balance (Crews and Ross, 1998; Guillette and Milnes, 2001).

Algal toxins Algal toxins are released by blue algae, which tend to produce blooms under conditions of eutrophication, and in marine environments by marine algae causing red tides. No published reports could be found of crocodiles having been affected by these events. However, the possibility exists of crocodiles being poisoned under such circumstances, and this should be borne in mind when investigating deaths of crocodiles in the wild.

Fire ants Radionuclides Radioactive contaminants may accumulate in the vicinity of atomic power stations. No ill effects have been documented concerning crocodilians living in contaminated reservoirs, but the accumulation of radiocaesium levels in crocodile tissues could be of concern as far as human consumption of crocodile meat is concerned (Brisbin et al., 1998). The re ant, Solenopsis invicta, has, since its introduction into the USA, established itself throughout the south-eastern states, often nesting in alligator nests. The effects of re ants on alligator eggs and hatchlings have been investigated by Allen et al. (1997). As soon as eggs begin to crack, the ants can penetrate the shell and consume the contents. Hatching alligators are bitten during hatching, until they are taken by the mother and placed into the water. When the hatching process was fast, the effects of the bites were not too severe. Swellings occurred mainly around the eyes and on the extremities.

Algicides A captive spectacled caiman developed visceral gout and died after its tank had been treated with an algicide containing streptomycin (Jacobson, 1984) (see also below).

Botulism Botulism is caused by the toxins of Clostridium botulinum. The agent grows under anaerobic conditions in the mud of eutrophicated water bodies or in cadavers. It remains active in animals that have died from botulism. In the mud the toxin is accumulated by invertebrates and, when taken up by water fowl, can produce heavy mortality amongst these birds. The toxins cause a accid paralysis of all limbs as well as the neck. If the type of toxin can be determined, the patient can be treated with the appropriate antitoxin. A case of suspected botulism in 8 out of 800 juvenile Indo-Pacic crocodiles was reported by Youngprapakorn et al. (1994).

Rodenticides No cases of rodenticide poisoning have apparently been reported. However, most rodenticides contain anticoagulants, which remain active in the killed rats and can subsequently affect the predator catching and eating the poisoned rats. A monitor lizard residing in the roof of our house died in this way. Since rats are attracted into the crocodile pens by left-overs of food, and are possibly eaten by crocodiles, there is the danger of accidentally poisoning young crocodiles, which most likely would die from massive internal haemorrhages (see p. 219).

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The animals were paralysed and lacked pupillar reexes, but they also suffered from spasms, causing the limbs to become rigid. The report therefore has to be treated with some caution. One of the photographs shows an animal with very diaphanous teeth, indicating that this might, in fact, have been a case of hypocalcaemia (see p. 211).

Antibiotics Resistance Antibiotics are used to suppress bacterial growth in infections. However, a prolonged exposure selects for resistance in the surviving bacteria to the specic antibiotic or to a class of antibiotics. This resistance can be passed on to other species of bacteria as well. While this is not a toxic effect in the strict sense of the word, it is a deleterious effect, which needs mentioning. Crocodiles are not only exposed to the antibiotics that are given to them prophylactically or therapeutically, but also to those present in carcasses and organs of farm animals fed to the crocodiles. Residues of antibiotics may render crocodile meat unt for human consumption. Gentamycin Gentamycin is known to be nephrotoxic and reptiles are particularly vulnerable to overdosing with this antibiotic because of their slow metabolism (Montali et al., 1979; Knox, 1980). Structural damage to the kidney tubules reduces the ability of the kidneys to eliminate uric acid and causes gout, the accumulation of uric acid crystals (see p. 230). As Aeromonas hydrophila often is sensitive to gentamycin, veterinarians are tempted to use it in cases of septicaemia (see pp. 173 and 228), and this author admits having unintentionally killed juvenile crocodiles with repeated gentamycin injections. Streptomycin Streptomycin has been blamed for causing the death of a captive spectacled caiman following treatment of its tank with an algicide containing this antibiotic (see also above) (Jacobson, 1984). Ivermectin At one-half of the mammalian dose, ivermectin causes paralysis in Nile crocodiles (personal communication, C.M. Foggin, Harare, 2000). There is a suspicion that it is also toxic to other crocodilian species.

Vitamin D With on-farm mixing of rations by many crocodile farmers there is the possibility of inadvertantly adding too much vitamin premix. Usually no mixing records are held. Excessive vitamin D consumption by North Pole explorers who ate the livers of polar bears caused severe problems, with abnormal bone formation in soft organs and exostoses. Vitamin D is also used to poison warfarin-resistant rats. In green iguanas, hypervitaminosis D caused calcication of the aorta and pulmonary arteries (Pallaske, 1961; Wallach, 1966), as well as degeneration of the kidneys, with a hyaline to ground-glass appearance on the cut surface (Wallach, 1966). Such cases of hyaline degeneration of the kidneys were seen in adult farmed Nile crocodiles that had died from stress septicaemia (see p. 228) after having been translocated to a new breeding enclosure during winter (Fig. 7.29) (authors own case). The muscular ossication seen by Youngprapakorn et al. (1994) most likely is caused by displaced embryonic tissue, while the muscular calcication described in the same publication could have been a sequel of Zenkers degeneration (see p. 219). The report of suspected vitamin D poisoning in farmed Nile crocodiles by Huchzermeyer (1999) was in error; it was a case of osteoporosis (see p. 211). To prevent any possible toxic effects, vitamin supplements should be given according to recommendations and not be overdosed. Since this vitamin is stored in fat, it may also be necessary to take into consideration the vitamin D status of dead poultry fed to the crocodiles.

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Anti-inammatories Probenecid, phenylbutazone and salicylates inhibit the secretion of urates and cause gout (see pp. 230 and 264) (Cardeilhac, 1981).

Mycotoxins Mycotoxins, and possibly also a vitamin B1 deciency (see p. 217), were suspected to be responsible for cases of severe fatty degeneration of the liver in farmed juvenile and adult spectacled caimans (Villafae et al., 1996) (see also p. 261). However, fatty degeneration of the liver is commonly present in anorectic and runting crocodile hatchlings (p. 234).

Multifactorial Diseases
Multifactorial diseases are man-made diseases, typical of intensive husbandry conditions and, in crocodiles, also of conditions of captivity. These diseases are caused by the combined actions of several factors, and in many instances it is difcult, or even impossible, to assign a leading role to any of the factors involved. Since the concept of multifactorial diseases is relatively new, they do not t into the traditional way of describing diseases, which are classied by their only, or main, cause. This leaves the multifactorial diseases to be dealt with somewhere towards the end of the book, whereas according to their importance they should have their place right in front. It is hoped, though, that the reader will nd this section, and will not study it less than the preceding ones. The factors involved in multifactorial diseases are all the ones commonly associated with captive or intensive farming conditions. Without doubt, the single most important factor in all the conditions in this section is stress, and since stress does not t into the standard classication either, it will be discussed in detail in Chapter 7 (p. 278). Other factors playing an important role are malnutrition, accumulation of microorganisms in the immediate environment and immune suppression by unsuitable temperatures.

In very simple terms, one can also try to explain this concept as interactions between the environment (physical, chemical and biological) and the organism (in our case the crocodile with its defences) (see p. 46). Among the physical factors are temperature and sources of heat, as well as humidity, light and noise. Important chemical factors are water and air quality, disinfectants and other chemicals used on the farm, as well as contaminants. Biological factors range from microorganisms in environment and food, via the food itself, to intraspecies interactions and the human presence. The different factors in the environment exert a pressure on the crocodile, which responds to these pressures with its defences (see Fig. 1.47). As long as the defences are adequate, there is a balance, and a crocodile in balance with its environment is healthy. If a single, or the combined, pressures become too strong for the defences of the crocodile, there will be an imbalance, and this imbalance will cause disease. In the sense of the discussion above, the defences of the crocodile do not only consist of the physical barriers of skin and mucosae and of the immune system, but of the whole gamut of physiological, biochemical and behavioural adaptations of the crocodile to life in its specic ecological niche. The success of keeping crocodiles in captivity, or in an intensive farming system, depends on the degree to which we are able to cater for these specic adaptations.

Enteritis Aspects of this subject have already been dealt with under hatchling diseases (see p. 145). In the following the emphasis will be on the multifactorial aspects of the disease. The factors involved in causing enteritis are: intestinal ora; inadequate temperature; stress; bacterial infection from unhygienic meat; bacterial build-up in the environment; viruses.

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Intestinal ora Very little is known about the normal intestinal ora of crocodiles living in the wild. Our limited knowledge is summarized in Chapter 1 (p. 38). In all animals the normal intestinal bacteria occupy the available attachment sites on the epithelial surface of the intestine and, with their metabolism, produce an environment not conducive for the establishment of pathogenic bacteria. This process is known as competitive exclusion. Fungi also are part of the normal intestinal ora. In nature, the intestinal ora derives from the nest, from the water in the nursery contaminated with the faeces of the mother and also from the live food eaten. In the sterile environment of the hatchery, and under severe hygienic conditions in the rearing house, a hatchling may not be exposed to the normal intestinal bacteria it requires and may therefore not be able to establish the required intestinal ora. Antibacterial treatment during this period may further limit the range of available bacteria, and may strongly favour fungi. The bacteria available under these circumstances are either highly resistant to antibacterial treatment and hygiene measures (e.g. Pseudomonas spp.), or they derive from the food, raw minced meat, particularly if it is prepared from livestock farm mortalities (e.g. salmonellae and pathogenic Escherichia coli). This obviously opens the door to outbreaks of enteritis. Cultures of intestinal bacteria suitable for the initial colonization of the gut are called probiotics. Probiotics based on a single species are less effective than those containing several bacterial species. No crocodilespecic probiotics are presently available, but several poultry products are, and these could be used to treat hatchlings. However, included under the name of probiotics are also preparations made from dead bacteria, which are used only for their enzyme action. These preparations usually contain vitamins as well. Only probiotics based on live bacterial cultures should be used for the purpose of gut colonization of hatchlings, or of older juveniles after antibacterial treatment.

The individual bacterial and fungal species also have temperature optima, which allow them to function well. It is therefore possible that keeping crocodiles at constant high or low temperatures already limits the number of bacterial species able to thrive in the intestinal environment.

Inadequate temperature Crocodiles have certain temperature requirements, depending on their activity, and they try to adjust their body temperature accordingly (see pp. 44 and 55). Inability to achieve the desired temperature causes stress (see below), as do overheating or excessive temperature uctuations. Low temperatures reduce the activity of the immune system. Any of these conditions can contribute to lowering the resistance of the crocodiles and to triggering an outbreak of enteritis. Stress Repeated, ongoing and/or severe stress reduces the functions of the immune system (see p. 278). Temperature stress has been discussed above. A further source of stress commonly found on crocodile farms is fear, the inability of hatchlings or juveniles to nd cover. Even in a closed rearing house, the crocodiles do not recognize the ceiling as cover. To feel secure they need something much lower to creep under, e.g. hide boards (see p. 114). Any disturbance, handling, etc. can also cause stress, as does overstocking (see p. 116). Bacteria The main source of bacterial contamination and infection is the feed. Even pelleted feed is not sterile and can contain salmonellae. However, raw meat, particularly minced meat, of farm fatalities is the most important source of pathogenic bacteria. Initially, these may infect one single crocodile and multiply in its gut. Excreted with the faeces, they then contaminate the environment. The warm and nutrient-rich water in the rearing house

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allows further multiplication of the bacteria in the periods between water changes. A thin layer of fat on the surface of the water collapses on the oor, when the water is drained. This fat is not removed by normal scrubbing. Under it, bacteria nd protection from supercial cleaning and disinfection. In this manner the bacterial contamination of the rearing house can build up. Further sources of bacterial contamination are the faeces of rats and ies attracted to the crocodile feed in open rearing facilities. Other organisms Coccidia cause a specic enteritis, dealt with elsewhere (see p. 183), but coccidial enteritis can be complicated by bacterial infection. The other presently known intestinal protozoa can mostly be regarded as harmless (see p. 190). Adenovirus can cause enteritis, and this infection can also be complicated by, or predispose to, bacterial enteritis (Foggin, 1987). It is presently unknown whether Paramyxovirus can cause enteritis in crocodiles (see p. 162). Clinical symptoms and pathology Diarrhoea is rarely seen because of the prevalently exudative reaction, which frequently leads to an occlusion of the intestine the affected hatchlings lose condition and have a bloated appearance (see also p. 145). The different pathological manifestations are described in Chapter 7 (p. 255). Treatment On the one hand, the treatment of enteritis must be based on the diagnosis of the bacterial agent involved and its antibiogram, but, on the other hand, one has to consider the other factors as well. Correct the temperatures, reduce other sources of stress, reduce contamination of feed and environment and instigate a cleaning and disinfection programme that will prevent a recurrence of bacterial build-up in the immediate environment of the crocodiles.

Prevention The prevention of enteritis is fourfold: establishment and maintenance of a normal and protective intestinal ora; optimal temperature conditions; stress-free rearing conditions; and a hygiene programme preventing bacterial build-up.

Septicaemia Crocodiles, not having any lymph nodes, are prone to the rapid spread of bacteria into the blood circulation septicaemia. The danger is somewhat limited by the peculiarity of the prevailing inammatory response, exudation, which tends to immobilize invading organisms in localized infections, preventing them from draining into the blood circulation and causing septicaemia (p. 46) (Huchzermeyer and Cooper, 2000). This leaves the intestine as the main source of infection and port of entry to the general circulation. The bacteria that have been found in cases of septicaemia have been listed in Chapter 5 (p. 173). The factors involved are stress, temperature and the intestinal ora. Bacterial translocation Individual bacteria of the intestinal ora are transported through the intestinal mucosa at the sites of gut-associated lymphatic tissue, and presented as antigen for the production of local antibodies; or are transported by macrophages into the circulation and presented as antigen for the production of humoral antibodies (Neutra, 1998; VasquezTorres et al., 1999). Apart from this, the barrier between the intestinal ora and the blood, the mucosal barrier, remains intact in a healthy animal. However, at least in ostriches and crocodiles, this barrier can break down under conditions of severe stress, allowing a few bacteria access to the blood circulation (authors own unpublished observations). In human patients it has been established that bacterial translocation from

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the gut occurs after trauma or burn shock (Deitch et al., 1996) and nitric oxide plays a role in the regulation of this process (Nadler and Ford, 2000). Chance or opportunity determines which bacterial species is translocated, and consequently there are no bacterial species that are particularly selected by this process. Under favourable conditions, and if the stress does not persist, the immune system quickly eliminates the invaders. If stress conditions prevail over a longer time, suppressing the activity of the immune system, or if the immune system is incapacitated by cold, the invading bacteria can thrive and multiply. As the liver lters the blood returning from the intestine through the portal system, the bacteria may provoke varying degrees of cellular reaction and even a severe hepatitis. The bacteria may also invade the joints or serous cavities, causing arthritis (Huchzermeyer, 2002) (see also p. 273), pericarditis and polyserositis (see p. 269). Clinical signs At rst the affected crocodile(s) may behave and feed normally. In the longer run, as various organs become affected, symptoms may develop accordingly. This may take weeks. Crocodiles that have been stressed during a period of cold weather (capture and translocation in winter) may not regain their appetite with the onset of warmer weather. In advanced stages, juvenile crocodiles often show a reddish discoloration of the ventral skin (see Plate 9). Subadult crocodiles often present with whitish patches on the facial skin, particularly around the nostrils and the eyes (see Fig. 5.17). We used to call this white nose disease and in conjunction with gastric ulcers rhinogastritis (Huchzermeyer and Penrith, 1992) (see also p. 237). In the nal stage, all affected crocodiles become lethargic, often refusing to go into the water (see p. 290). Pathology In acute cases, the animals will be in good nutritional condition, while the lesions may depend on the bacterial species involved and on the localization of the infection. They

include severe diffuse or focal hepatitis (see p. 259), subcutaneous haemorrhagic oedema, myocarditis and acute brinous epicarditis (see p. 269) (Ladds and Sims, 1990). Splenomegaly is commonly seen in chronic cases, except in emaciated individuals (Huchzermeyer, 1994) (see also p. 270), as are granulomatous lesions in the liver. Because of the continuous perfusion of liver and kidneys, there is always some degree of lymphocytic reaction in these organs. Gastric ulcers may be present, and in some cases these may be colonized by ascaridoids (p. 192) (Huchzermeyer and Penrith, 1992; Huchzermeyer and Agnagna, 1994; Ladds et al., 1995). Treatment Any antibacterial treatment will have to be based on bacterial isolation and an antibiogram, in individual cases from a blood sample. However, any handling of the affected crocodile(s) may cause further stress and further aggravate the problem. Small hatchlings appear to be more tolerant of handling and can be dosed orally with a nutrient uid containing the chosen antibiotic (see pp. 86 and 148). Prevention It is most important to avoid severe, continuous stress, particularly if the animal will be unable subsequently to maintain an optimal body temperature. Crocodiles should never be captured and transferred in winter. Where such an action is unavoidable, the crocodile should be given a prophylactic treatment with a broad-spectrum antibiotic. Because of the suspected role of nitric oxide in the bacterial translocation, and because of the oxygen scavenging action of vitamin C and its role in supporting phagocytosing macrophages, prophylactic treatment with ascorbic acid may also be appropriate (see also p. 218).

Generalized fungal infections The mechanisms causing stress septicaemia seem to apply to generalized fungal infections as well (see p. 182). They also are seen

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frequently after severe stress, and particularly in association with cold. Some fungi are known to be able to multiply under cold conditions, when many bacteria become dormant. Consequently, generalized mycosis is typically a spring disease. It develops during winter and nally kills the crocodile in spring.

Gout Uric acid is one of the end-products of protein metabolism (see p. 48). Its solubility is limited. As soon as plasma uric acid levels rise beyond saturation, uric acid crystals begin to form. Gout is therefore characterized by the deposition of urate crystals in the kidneys, on serous surfaces of the internal organs, in the joints, throughout the musculature and even in the stomach, due to the inability of the kidneys to excrete all, or the excess, urates. The localization of the deposits varies from case to case. Factors involved in causing gout are nutrition, dehydration, cold, stress, infection and toxic substances. Nutrition The natural diet of crocodiles is rich in protein, and under normal circumstances the kidneys should be able to cope with the output of uric acid from protein metabolism. However, if protein has to serve as source of energy as well, there may be an excess production of end-products of nitrogen metabolism. Nitrogen excretion in the form of ammonia, as well as uric acid, was higher in American alligator hatchlings fed maximally on ve meals per week than in those fed a single meal after a fast, with lower uric acid clearance and higher uric acid plasma levels in the latter group (Herbert, 1981). This appears to be in contrast to the common assumption that overfeeding is one of the causes of gout in farmed crocodilians (McNease and Joanen, 1981). As mentioned above, the energy value of the ration may play a role in this. Kidney pathology caused by vitamin A deciency was found to be responsible for

outbreaks of gout in farmed crocodiles (Foggin, 1987; Ariel et al., 1997a) (see also p. 216). High calcium supplementation has also been mentioned as a suspected cause (Foggin, 1992a). However, it seems unlikely that the feeding of fatty sh or meat could cause gout (Pooley, 1986). Intermittent feeding, as discussed above (Herbert, 1981) and as it may occur in captive situations, particularly in association with lower temperatures (see below), may well be more important than the composition of the feed itself. Dehydration Dehydration not only decreases the ow through the kidneys and thereby their output, but also leads to a certain concentration of the plasma (Cardeilhac, 1981). Because of the low solubility of uric acid, this can then trigger the formation and deposition of uric acid crystals. Dehydration may occur during prolonged transport. Fed animals are more susceptible to the effect of dehydration than fasting ones. All farming operations should be run in such a way that dehydration cannot occur. Cold Gout occurs more commonly during the winter months (Pooley, 1986). This has to do not only with an inability to metabolize digested food at lowered temperatures, but also with the lower solubility of uric acid at lower temperatures. Under certain farming or captive conditions, crocodiles that have been warm during the day and have eaten their ll and then have started to digest and metabolize, raising uric acid plasma levels, will be forced to cool down during the night, causing uric acid crystals to form. American alligators may be protected from this effect of cold by the seasonal suppression of appetite (see p. 37). Stress There is only an indirect action of stress in the aetiology of gout, via stress septicaemia (see p. 228) causing kidney infection and nephritis (see below). There could possibly be another action, via disturbed behaviour

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interfering with thermoregulation and normal water intake (see p. 289). Infection The continuous high rate of perfusion makes the kidneys vulnerable to bacterial infections in cases of septicaemia (see p. 228). Infection and inammation interfere with the function of the kidneys, causing uric acid crystal deposition, often in the affected kidneys themselves. Cases of pyelonephritis in Crocodylus novaeguineae (Ladds et al., 1995) and in C. johnsoni (Buenviaje et al., 1994) could also have been triggered by an ascending infection. The latter case was complicated by a vitamin A deciency (see above). Toxic substances One case of gout in a captive crocodile was apparently caused by the use of an algicide containing streptomycin (Jacobson, 1984) (see also p. 224). Other nephrotoxic substances are the antibiotic gentamycin (Knox, 1980) (see also p. 225) and certain antiinammatories such as phenylbutazone, probenecid and salicylates (Cardeilhac, 1981) (see also p. 226). The experimental ip injection of the amino acid D-serine caused renal failure with the production of small quantities of pale urine, plasma uric acid concentrations of 70 mg per 100 ml and massive deposition of uric acid crystals throughout the body (Coulson and Hernandez, 1964). Birth defects Congenital gout occurred in two subsequent years in a number of Nile crocodile hatchlings from eggs collected from an area on Lake Malawi. The hatchlings lived a short time only and showed gout deposits around their joints (Foggin, 1992a) (see also p. 155). Kidney aplasia: occasionally only one kidney develops and, although it is larger than a normal paired one, it may reach a stage when it can no longer cope with the high metabolic demands placed on it in a farm situation, and consequently gout develops (see also p. 155).

Species involved While one would presume that all crocodilian species would be equally susceptible to gout, it has to be noted that, in mixed farming operations, Crocodylus porosus were not affected, whereas C. novaeguineae and C. johnsoni suffered cases of gout (Buenviaje et al., 1994; Ladds et al., 1995). Other species from which cases of gout have been reported are: farmed American alligators (Cardeilhac, 1981; McNease and Joanen, 1981); a captive spectacled caiman (Jacobson, 1984); farmed Nile crocodiles (Pooley, 1986; Foggin, 1987); a wild adult Indo-Pacic crocodile (Buenviaje et al., 1994); a captive false gharial (Frank, 1965); a captive gharial (Frank, 1965).

Clinical signs In all cases of gout there is a general depression. In renal gout, the swollen kidneys exert pressure on the sciatic nerves, causing a hind limb paralysis; while in arthritic gout, the affected leg joints become painful and the animal is reluctant to move. In advanced cases of arthritic gout, the swollen joints can be seen or palpated. A needle aspirate from such a joint will contain the white paste of uric acid crystals, and analysis of a blood sample will show elevated uric acid levels (see p. 47). Pathology Macroscopically, the most obvious lesions are the gout deposits on the serous surfaces, particularly the pericardium and epicardium, in the joints, throughout the musculature, in the stomach and in the kidneys, the localization varying from case to case (Figs 6.146.17, Plate 16). The actual distribution of these deposits may depend on a number of factors: in cases of nephritis and pyelonephritis the deposits are mainly in the kidneys. The somatic distribution may depend on thermal conditions. Cold, lower-

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Fig. 6.14. Gout in a farmed Nile crocodile: uric acid deposits on the epicardium.

Fig. 6.15. Gout in a farmed Nile crocodile: uric acid deposits in the joints of the four legs.

ing the solubility of uric acid, may cause its precipitation in the leg joints, when in uctuating temperatures the legs cool down more rapidly than the body. The uric acid crystals can best be recognized in a direct smear under a polarizing microscope. Often the formalin used for x-

ing the histopathology specimen dissolves the crystals, leaving only the urate clefts in the tissue. Tophi (the collection of urate crystals) may be surrounded by an inammatory reaction with multinucleated giant cells (Youngprapakorn et al., 1994; Ariel et al., 1997a).

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Fig. 6.16. Gout in a farmed Nile crocodile: uric acid deposits in the musculature.

Fig. 6.17. Gout in a farmed Nile crocodile: uric acid deposits in gastric ulcers.

Squamous metaplasia and hyperkeratosis of the large collecting ducts in the kidney were found in gout cases caused by vitamin A deciency (see above) (Foggin, 1987; Ladds et al., 1995; Ariel et al., 1997a) (see also p. 216). Treatment Only early cases of gout can be treated, and the possibilities of treatment are limited to rehydration in cases of dehydration (Knox,

1980) and fasting for 1 week to 10 days in cases of overfeeding (Cardeilhac, 1981; McNease and Joanen, 1981). Prevention For the prevention of gout it is important to avoid all the factors contributing to its aetiology, but particularly not to feed when low temperatures are expected, and also not 48 h before capture and transport. Dehydration has to be avoided under all circumstances.

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Runting Runting is the failure of some crocodiles in a group to grow. This can be seen in hatchlings and in juveniles, and it can be caused by a large number of factors. Under certain conditions runting can be the cause of a major proportion of farm mortalities (Buenviaje et al., 1994). Factors involved Primary anorexia occurs in hatchlings that never learn to feed, while secondary anorexia may be caused by certain rations, e.g. sh (Foggin, 1992a) or unpalatable rations in general (McInerney, 1994). However, anorexia is a special case (see pp. 283 and 289), as anorexic hatchlings do not recover and therefore starve to death in a slow, protracted process, while true runts continue to eat but fail to grow or grow only very slowly. There may be genetic causes in some cases of runting, and poor incubation conditions may also play a role (Peucker and Mayer, 1995). Hatchlings from small eggs laid by young females will be smaller than average and may be disadvantaged from the start. Of the environmental factors, temperature is probably of major importance. Nile crocodile hatchlings kept at 25C lost weight although they continued to feed (Kanui et al., 1991). Generally, the inability to maintain an adequate temperature on a thermogradient, exposure to severely uctuating temperatures and overheating are very stressful (see p. 278). Other sources of stress are a high stocking density, bullying by larger individuals and the inability to hide, and fear. As a major cause of runting, these have been summarized as adaptation failure (Buenviaje et al., 1994). Some of the runts appear to be afraid to go into the water and, rather, try to hide in a corner of the pen, where they dehydrate (Foggin, 1992a) (see also p. 289). This dehydration further aggravates their condition. Poor yolk-sac absorption may be linked to poor incubation conditions but also to inade-

quate temperatures or even yolk-sac infection (see p. 147). Nutritional factors may either have something to do with the palatability of the food (see above) thereby limiting feed intake, its composition or with poor protein assimilation and prolonged stomach clearance (Davenport et al., 1990). The latter may also be the case in hatchlings recovering from an adenovirus infection (Foggin, 1987, 1992b) or other intestinal infections, such as coccidiosis (see p. 183), while a complete intestinal occlusion by exudate after coccidiosis or salmonellosis (see p. 164) will lead to death by starvation. An immune deciency suggested by Foggin (1987) may well be caused nutritionally by a poor feed intake. Clinical signs The most obvious sign of runting is the failure to grow in comparison to other individuals in the same group. The neck becomes drawn in, while the abdomen may or may not appear distended against the emaciated body (Fig. 6.18). Blood taken from runted Nile crocodiles had lower haemoglobin and packed cell volume values than blood from normal ones, and elevated alanine transaminase and alkaline phosphatase values (Foggin, 1987). Runted C. porosus hatchlings had elevated alanine A-transferase, aspartate A-transferase and alkaline phosphatase values (McInerney, 1994) (see also p. 47). Pathology The pathology ndings are non-specic, with emaciation, depletion of the abdominal fat body (see p. 28), atrophy of liver and intestine and sometimes ascites. The liver has a greyish colour, with fatty and vacuolar degeneration and increased numbers of melanomacrophages histopathologically. In the pancreas there is an atrophy of the acinar cells (Foggin, 1992a). Treatment First of all it must be realized that runting is mainly due to conditions on the farm, not so

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Fig. 6.18. Runted Nile crocodile hatchling with distended abdomen.

much maladaptation (Buenviaje et al., 1994), but rather a failure to provide suitable conditions (see above). Unless the factors involved on the particular farm are diagnosed correctly and subsequently rectied, any possible treatment will be of rather limited value. This should be the work of the consulting veterinarian. As long as the veterinarians role remains restricted to the laboratory and to prescribing antibiotics, no solutions will be possible for any of the multifactorial diseases. Runts should be separated from larger hatch mates to prevent further bullying. They can then be force-fed by stomach tube (see p. 86) with a nutrient liquid twice a week at 20 ml kg 1 body mass. Such a liquid could be made by homogenizing 250 g of fresh sh in 250 ml water with the addition of 1 ml concentrated multivitamin drops (Foggin, 1987) or, my own formula, by mixing one egg yolk with 10 ml milk and 5 g of sugar. A single im multivitamin injection appeared to have a benecial effect (Peucker and Mayer, 1995), while the treatment of normal Nile crocodile hatchlings with a recombinant human growth hormone had a temporary effect only, with cessation of feed-

ing a week after the treatment was halted and subsequently even loss of weight (Andersen et al., 1990). Rehydration of dehydrated animals may be problematical. Simply forcing them into water and preventing them from coming out on to land may cause further stress and, furthermore, interfere with their thermal requirements. Force feeding dehydrated runts with a very dilute nutrient liquid (equal parts of water and of one of the above formulas) may be a better approach. Unless treatment is given early, the prospect of success is rather limited. Survivors may resume growing but at a very reduced rate, never reaching a suitable size for slaughter. Prevention The large-scale incidence of runting is entirely preventable. All the factors cited above should be examined carefully, but of particular importance are stocking density, the provision of a suitable temperature regime and a stress-free environment. Even the palatability of the ration becomes less

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important when all the other factors have been corrected.

Winter sores Winter sores occur in older juvenile crocodiles that are exposed to cold winter conditions. Under such conditions, the blood ow to the skin is reduced and the immune system is functioning only suboptimally. This allows bacteria from a contaminated environment, mainly of faecal origin, to take a hold in minor scratches, particularly in the soft tissue between the scales. The lesions caused by these local infections are covered by yellow-brownish crusts (Plate 17 and Fig. 6.19). Winter sores typically occur on farms where the hatchlings have been reared for their rst year in a heated environment but, due to lack of space, are placed in outside pens in their second year. Factors involved The two main factors are insufcient temperatures for the local and humoral immune system to function optimally, and unhygienic conditions. Outside ponds used for accommodating juvenile crocodiles in winter are usually deeper, to protect the crocodiles against

excessive cooling. However, the water in such a deep pond is not changed daily, nor are cleaning and disinfection carried out on a daily basis, and this can lead to a severe accumulation of faecal matter in the water. Since the crocodiles are not fed during the cold months, latent vitamin deciencies may also develop. Overcrowding is often seen under these conditions as well, as during the summer the crocodiles may already have outgrown the available space. This causes stress, which further depresses the immune system. Clinical signs Affected crocodiles have yellow-brownish crusts between the scales, particularly on the ventral skin. These crusts usually are no larger than c. 5 10 mm. They are larger and lighter in colour than those seen in cases of crocodile pox (see p. 158), but similar to those seen in dermatophilosis (see p. 172). Pathology Macroscopically, there are supercial lesions covered by yellow-brownish crusts. Histopathologically, there is a destruction of the epidermis and an accumulation of round cells in the dermis. The crusts are formed by necrotic cells and bacteria (Huchzermeyer, 1996c).

Fig. 6.19. Winter sores on the ventral surface of the neck and thorax of a juvenile Nile crocodile.

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Permanent scarring can cause the skins of affected crocodiles to be downgraded. Bacteriology Bacterial cultures from the lesions produce a large variety of non-pathogenic, potentially pathogenic and known pathogenic bacteria in mixed culture from every single specimen (Huchzermeyer, 1996c). Treatment The treatment of winter sores is based primarily on rectifying the conditions that initially caused them, particularly temperature and hygiene. For possible technical solutions to the problems caused by cold in outside rearing see Chapter 3 (p. 108). Once these conditions have been rectied, the healing process will start by itself. It can be assisted by daily spraying of the crocodiles, best at the time of water change, with a mild but effective disinfectant, such as F10 (Health and Hygiene, South Africa) at a dilution of 1:250. Prevention Winter sores can be prevented only by providing protection from cold in conjunction with adequate hygiene, consisting of regular water changes, scrubbing and disinfection, and the avoidance of overcrowding.

Factors involved Overcrowding of animals that are at the stage of developing their territorial behaviour is the most important factor. An unsuitable temperature regime and insufcient hygiene may also play a role. As the animals become anorexic, secondary nutritional deciencies further aggravate the condition, possibly causing a biotin deciency (Youngprapakorn et al., 1994). Clinical signs Affected crocodiles are listless and anorexic and develop the typical skin lesions, consisting of patches of white discoloration, starting around the nostrils, then spreading to the eyelids and, in advanced cases, affecting the whole body (Plate 18, Figs 6.20 and 6.21). Pathology Usually the affected animals become emaciated. The skin lesions range from supercial erosion and discoloration of the epidermis, to ulceration, accompanied by cellular inltration in the dermis (Fig. 6.22). There may also be an inammation of the apical parts of the nasal passages. Gastric ulcers, when present, are associated with polyarteritis (Huchzermeyer and Penrith, 1992). They are dealt with in detail in Chapter 7 (p. 251). A large variety of non-pathogenic and pathogenic bacteria can be isolated from the skin lesions. Treatment There is no successful treatment, unless the affected animals can be released into larger holding pens with suitable temperature conditions. For the treatment of anorexia, see Chapter 7 (p. 282). Improving hygienic measures and spraying the animals at least once a day with a suitable disinfectant (F10, Health and Hygiene, South Africa, diluted 1:250) may help to improve the condition of the skin. On valuable individual animals, a more intensive treatment could be tried, such as the one described in Chapter 7 (p. 253).

Chronic stress dermatitis Chronic stress dermatitis is characterized by the appearance of patches of whitish skin discoloration, particularly around the nostrils and eyes, but occasionally anywhere on the body. It is also referred to as white nose disease. It affects mainly older juveniles and subadults held in crowded indoor conditions, often involving the largest specimens in the group and particularly males. It is accompanied by steady deterioration, eventually leading to the death of the animal. Outbreaks occurring in conjunction with gastric ulcers have also been termed rhinogastritis (Huchzermeyer and Penrith, 1992).

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Fig. 6.20. Stress dermatitis: discrete erosions around the nostrils of a juvenile Nile crocodile.

Fig. 6.21. Stress dermatitis: lesions spreading to the eyelids of a juvenile Nile crocodile.

Fig. 6.22. Stress dermatitis: skin section showing cellular inltration in the dermis.

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Prevention Overstocking of larger juveniles and subadults often occurs when the construction of facilities for their eventual release has been falling behind schedule. This should be avoided at all cost. In the event of such delays, arrangements for alternative accommodation should be made in good time, and the crocodiles be moved before any losses occur.

Incidents of high mortality in wild crocodiles Incidents of high mortality in wild crocodiles appear to be rare. Adult crocodiles are very resistant, while many juvenile crocodiles rather fall prey to cannibalism. In any event, it is rare to encounter dead crocodiles in the wild. By the time a dead crocodile is found, the state of the carcass may have deteriorated to the point that it may no longer be possible to collect suitable laboratory specimens. The remoteness of most crocodile habitats also plays a role here. Specimens from a single carcass may not be representative of the entire outbreak of mortality, as was the case of an outbreak of high mortality in adult crocodiles with respiratory distress in Lake Rukwa in Tanzania in 1943, when only a few nodular skin lesions, presumably briscesses (see p. 46) were collected in formalin (Thomas, 1946). A less drastic, but very insidious, problem is posed by declining crocodile numbers in populations that otherwise may appear to be normal (Cardeilhac et al., 1998; Swanepoel et al., 2000). In such cases, environmental pollution has been suspected (for further details see pp. 221 and 223). With increasing human encroachment, the wild crocodile populations become less remote, but also more vulnerable. In the electronic age, communication becomes rapid and is available almost everywhere. It is therefore recommended that, in the event

of an outbreak of mortality in wild crocodiles, the advice of specialist veterinarians should be sought immediately and, if possible, a specialist veterinarian should take part in the eld investigation. He is best qualied to carry out the post-mortem examinations and to decide on which specimens to take for further laboratory studies. For details of the necessary equipment for such a eld investigation see Chapter 2 (p. 83). The multifactorial aspect of any such outbreak of high mortality should not be neglected in the investigation. Just to nd one particular pathogen may not be sufcient. The Aeromonas hydrophila and other bacteria found in dead alligators and other reptiles and sh in Lake Apopka in 1971 (Shotts et al., 1972) were not the primary pathogens. Rather, the infections were precipitated by environmental conditions, including eutrophication. If the multiple briscesses found in the one crocodile from the 1943 outbreak of mortality in Lake Rukwa (Thomas, 1946) were indeed representative of the situation, one possible explanation could be that soldiers stationed in the vicinity of the lake had been attracted by the excellent sh in the lake and had indulged in some grenade shing, which could have caused the multiple injuries, or even that an object in the lake had been used for artillery or bombing target practice.

Note Added at Proof


Osteoporosis (pages 211 and 281) More evidence has come to light linking osteoporosis and poor dental calcication to stress via lucocorticoids causing calcium depletion (authors own observations). This allows diaphanous teeth to be used as clinical indicator of chronic stress in captive and farmed crocodiles.

Chapter 7
Organ Diseases and Miscellaneous Conditions

Many of the conditions in this chapter have been dealt with in great detail in other chapters of this book, according to the causative agent(s). In all such cases the reader will be referred to the relevant chapters. This chapter should therefore be regarded as an aid to correlate clinical and pathological ndings with the specic diseases described in the preceding chapters.

Bacterial dermatitis There are several forms of bacterial dermatitis. Dermatophilosis is one of the two specic bacterial skin infections and has been diagnosed in Australian crocodiles as well as in American alligators (p. 172). An Erysipelothrix dermatitis occurred in a captive American crocodile (Jasmin and Baucom, 1967) (see p. 171). The other two known forms, winter sores, with yellowbrownish crusty lesions (pp. 236 and 241), and chronic stress dermatitis, with patches of white discoloration, particularly on the head around eyes and nostrils (pp. 237 and 241), are non-specic and many bacterial species can be involved. These latter two forms of dermatitis are multifactorial (see p. 226) and their treatment must be based primarily on the removal of the various causative factors.

Skin Diseases
Pox Pox is a viral infection of the skin. There are two different entities: caiman pox, with whitish crusty lesions (p. 157) and crocodile pox, with dark-brown crusty lesions (p. 158). Similar lesions, but rather yellow-brownish and slightly larger, have been found in dermatophilosis and brown spot (p. 172) as well as in winter sores (pp. 236 and 241). The diagnosis is based on the histopathology of the skin lesions, nding the typical intracytoplasmic inclusion bodies. There is no specic treatment. All one can do is try to reduce the impact of concurrent bacterial infections by giving a course of antibiotic treatment in the feed.
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Fungal dermatitis Fungal infections of the skin occur either locally or generalized under unhygienic conditions in animals with a reduced immune capacity due to stress or cold (see also p. 278). The different forms have been described on p. 177. Supercial infections in

CAB International 2003. Crocodiles: Biology, Husbandry and Diseases (F.W. Huchzermeyer)

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the epidermis do not provoke much of an inammatory response. Deeper infections cause a granulomatous reaction (Plate 19) and not an exudative one (briscess), as in the case of bacterial infections (p. 46). The treatment has, rst of all, to be based on an improvement of hygienic conditions, the reduction of stress and an improvement of temperature conditions. Supercial lesions respond very well to repeated spraying with the combination disinfectant F10 (Health and Hygiene, South Africa). The treatment of deep granulomatous lesions may need the application of systemic fungicides, such as ketaconazole. The provision of a hygienic, stress-free environment with a suitable temperature regime is most important for the prevention of fungal dermatitis. Furthermore, it must be emphasized that frequent or prolonged use of antibiotics in the feed destroys the balance of the intestinal ora and allows fungi to multiply out of control, which may lead to an abundance of fungal spores in the faeces and in the environment (see p. 176).

such as the reduction of scale numbers in the areas of the ventral skin where fore- and hind legs join the body, and double scaling. For obtaining a healthy skin it is necessary to add suitable vitamin and mineral premixes to the farm rations (see p. 99) and to avoid excessive temperature uctuations (see p. 111).

Winter sores Juvenile crocodiles exposed to cold temperatures for prolonged periods while held under unhygienic conditions are prone to bacterial skin infections which cause small to conuent yellow-brownish lesions between the scales (see p. 236). These lesions can cause permanent damage to the skin and will not heal unless environmental conditions are improved.

Chronic stress dermatitis white nose Larger juvenile crocodiles, and particularly subadults kept in cramped quarters, become listless and develop patches of white discoloration of the skin, particularly around the nostrils white nose and the eyes (Fig. 7.1). The lesions are caused by a supercial erosion of the epidermis (Youngprapakorn et al., 1994). This multifactorial disease has been described in detail on p. 237.

Parasitic dermatitis The most important skin parasites causing visible lesions, although not really an inammation, are the capillarid worms Paratrichosoma spp. (see p. 194), which burrow in the epidermis and cause visible meandering tracts that lead to downgrading of the affected skins. Fortunately, these parasites need earth ponds and cannot survive on crocodile farms and ranches where hatchlings and juveniles are kept in concrete-lined pens. Leeches congregating in the axillary lesions of Crocodylus johnsoni were believed to have caused puncture wounds in the axillary skin (Webb and Manolis, 1983) (see p. 203).

Skin injuries Scratches In older juvenile crocodiles, the large mandibular canine teeth often protrude above the level of the nose (see Fig. 1.20). When frightened crocodiles pile in the corner of a pen and one of the lower ones then pulls out, it scratches the belly skin of the crocodile above. Infection of these scratches can lead to permanent damage. Solutions to this problem have been sought by breaking off these canines, which quickly regrow, and even by trying somehow to repress the excessive growth of the teeth, the latter with-

Degenerative skin disease Nutritional and environmental factors, possibly also stress, may be involved in causing certain forms of degenerative skin disease,

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Fig. 7.1. White nose: erosions of the facial epidermis of a chronically stressed juvenile Nile crocodile.

out results as yet. The problem lies with piling, and this can be prevented by reducing fearful events and, even more importantly, by the provision of hide boards even up to slaughter (see p. 114). Strict hygiene, the frequent disinfection of the pens, will reduce the danger of scratches becoming infected. Supercial punctures Fighting in hatchlings may produce puncture wounds in the skin, which normally heal without even being detected. However, they can serve as point of entry of infectious agents, and in crocodile pox (see p. 158) lesions often are aligned in rows, indicative of an infection of puncture wounds (Plate 8). Abrasions While crocodiles walk out of the water, they always slide back into the water (see p. 35). This sliding on rough concrete may cause abrasions, particularly of the skin covering the ventral aspect of the mandibles and on the plantar surface of the feet (Figs 7.2 and 7.3). The plantar abrasions frequently become infected by fungi, causing granulomatous swellings (see below).

All concrete surfaces in crocodile pens should have as smooth a nish as possible. Frequent cleaning and disinfection of all concrete surfaces is also necessary to reduce the risk of infection.

Deeper skin wounds Bites and other wounds penetrating the dermis often become infected. Bacterial infection will elicit an exudative inammation and briscess formation (p. 46). These briscesses may continue to grow, eventually causing large swellings. They do not respond to antibacterial therapy. The only possible treatment would be radical excision of the briscess. Fungal infection of skin wounds elicits a granulomatous response. The excision of such granulomatous masses is a possibility (Ensley et al., 1979) (see also pp. 95 and 240). Systemic treatment with an antifungal agent such as ketaconazole might be an option. However, most important is the prevention of abrasions by having very smooth surfaces in the crocodile pen. An infection of the abrasions can be prevented by frequent cleaning and disinfection of all the concrete surfaces in the pen.

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Fig. 7.2. Abrasions on the ventral surface of the mandible of a juvenile farmed Nile crocodile.

Fig. 7.3. Abrasions on the foot pad of the left forelimb of a juvenile farmed Nile crocodile.

Greasy skin When fatty meat is fed to crocodile hatchlings, a thin layer of fat forms on the surface of the water. When the water is drained, this surface layer is deposited on exposed surfaces, including the skin of the hatchlings. It

also traps traces of the nutrient-rich water. With time, a multilayered deposit is formed in this way. On the concrete surfaces this deposit resists being washed down and forms a protective layer above bacteria and fungi, which are trapped between the layers. On the skin of the hatchlings the fungi start

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multiplying, either in the fatty layers only or penetrating into the upper layers of the epidermis. The affected hatchlings loose condition and become visibly ailing (see also p. 177). A whitish layer can be seen covering the dorsal skin of the affected hatchlings (see Fig. 5.18). The treatment of this condition consists of spraying greasy surfaces in the drained pen, and the crocodiles as well, with a detergent, hosing them down and then spraying surfaces and hatchlings with a disinfectant with strong fungicidal action (F10, Health and Hygiene, South Africa, diluted 1:250). This treatment should be repeated daily for 1 week. For the prevention of this condition it is important to monitor the build-up of a fatty layer on the concrete, simply by scraping with a ngernail, and to use detergents and disinfectants as often as necessary.

Skin necrosis A case of necrotic dermatitis was described from a juvenile Crocodylus porosus that had not eaten for a while, and which died from generalized bacterial infection. Whole scales were lifting off, and underneath there was a subcutaneous oedema. In addition to lesions in the internal organs indicative of septicaemia, there was diffuse necrosis of the subcutis and the underlying muscle, with nests of Gram-positive coccoid bacteria (Buenviaje et al., 1998b).

Ulcerative dermatitis Deep skin ulcers were found in crocodiles suffering from severe chronic cases of fat necrosis (Youngprapakorn et al., 1994) (see p. 219).

Factors affecting skin quality Mycobacterial dermatitis Cases of granulomatous mycobacterial dermatitis in farmed Indo-Pacic crocodiles were described by Buenviaje et al. (1998b) (see p. 170). There is no treatment for mycobacterial infections in crocodiles. Crocodile farming is aimed at producing high-quality products. By identifying various factors that can affect the quality of the skin, one can try to avoid some of the more common causes of downgrading. However, the post-slaughter treatment of the skins falls outside the scope of this book. The in vivo factors can be classied as: genetic, environmental, behavioural, nutritional and microbiological. Genetics Abnormal scale patterns are rare, but are not acceptable to the market. Their most likely cause is genetics. Adult or future breeding crocodiles showing such patterns should not be used for breeding. It may pay to submit the breeding crocodiles to a certain degree of genetic selection. Environment A cold environment predisposes crocodiles to skin infections, e.g. winter sores (see pp. 236 and 241); cold or excessive temperature uctuations may also be one of the possible

Dermatophilosis Dermatophilus spp. have been isolated from crusty lesions of the ventral skin from farmed American alligators and Indo-Pacic crocodiles (Bounds and Normand, 1991; Buenviaje et al., 1997, 1998a,b) (see p. 172). The latter author also conrmed the transmissibility of the infection. Similar crusty lesions are found in a common condition associated with cold, called winter sores (see p. 236). Dermatophilus spp. do not respond to antibacterial treatment. The prevention of the infection must be based on the application of strict hygiene, particularly regular, thorough cleaning and disinfection of all surfaces in the rearing facility.

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causes of double scaling. Overheating is probably the main cause for the loss of scales in the axillary and inguinal regions of the ventral skin. Rough surfaces may damage the skin directly (see p. 241), they may also protect infectious agents from the effects of cleaning and disinfection (see p. 243). Nearideal environmental conditions are necessary for the production of top-class skins. Behaviour Fear-induced piling can cause scratches on the ventral skins of the piled crocodiles (see p. 241). Overcrowding may induce ghting, and also may cause severe stress leading to chronic stress dermatitis (see p. 237). It is important to pay attention to the behavioural requirements of the growing crocodiles. Nutrition No particular vitamin or mineral deciencies have been proven to cause skin defects in crocodiles, but this is due to the lack of experimentation. As in other livestock species, the requirements for supplementation certainly exist. It is safest to provide a nutrition supplemented with vitamin and mineral premixes designed for use in crocodiles (see p. 99). Using poultry premixes may not be sufcient, as the requirements of poultry are believed to differ from those of crocodiles. Overfeeding may lead to excessive fat in the abdomen, causing the skin to be stretched, with wide gaps between the scales. It is the energy portion of the ration, particularly the fat, that causes excessive deposition of abdominal fat. A fat body:heart ratio of more than 5:1 indicates that the crocodiles are fed a ration with an excessive energy level (see p. 85). A lean crocodile produces a better skin. Infection There are many infections, including at least one form of parasitism, capable of causing permanent damage to crocodile skins. These conditions have been dealt with above. Their prevention is of the utmost importance. The

role of thorough cleaning and disinfection cannot be overemphasized. Factors unknown There has been an increasing incidence of pitting in tanned American alligator skins. These pits cannot be detected on untanned skins. Consequently their later downgrading constitutes a loss to the trade. The cause of this pitting is still unknown (Haire, 1997). A no-no In spite of all the emphasis on skin quality, there is one action that has to be avoided, an absolute no-no: the examination of the ventral skin of the live crocodile before slaughter! It is immaterial in any case, as the crocodile is going to be slaughtered sooner or later anyhow and any visible defects are not going to heal before then. However, catching and handling the crocodile before slaughter causes severe stress, inducing stress septicaemia, where intestinal bacteria enter the blood circulation, leading to contamination of the meat with these very same intestinal bacteria, including salmonellae (Huchzermeyer, 2000) (see pp. 125, 164, 228 and 278). Crocodile meat should be marketed as a high-quality product and this must be considered in the overall production process.

Eye Diseases
Conjunctivitis Conjunctivitis is the inammation of the conjunctivae, the mucosal lining of the internal surface of the two external eyelids and both surfaces of the third eyelid, as well as the conjunctival sac. The inammation can be serous, with increased lacrimation (Villafae et al., 1996), or exudative (see p. 46). The serous inammation may extend into the nasal passages, causing rhinitis (Villafae et al., 1996). An exudative conjunctivitis causes blindness due to the accumulation of brinous exudate behind the eyelids.

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One-eyed Conjunctivitis affecting one single eye may be caused by injury or by a foreign body lodging in the conjunctival sac or behind one of the eyelids. A non-spreading infection, particularly a fungal infection, can also be limited to a single eye. A few cases of one-sided conjunctivitis were seen in outbreaks of meningitis (see p. 267) caused by Providentia rettgeri (see p. 174) in farmed C. porosus (Ladds et al., 1996). Repeated cases of one-sided conjunctivitis in captive juvenile American alligators (Fig. 7.4) have been ascribed to ant bites, or to the irritation caused by ant bites and subsequent scratching (S. Martin, Pierrelatte, 2002, personal communication).

Two-eyed Conjunctivitis affecting both eyes, but only in individual animals, is caused most likely by non-specic bacterial infection. Such cases have been seen in farmed crocodiles in Irian Jaya with brinous exudation (Ladds et al., 1995) and also in Australia (Hibberd et al., 1996). Outbreaks of conjunctivitis are due either to exposure to an irritant substance in the

environment or, more likely, to specic infection. Outbreaks of serous conjunctivitis, associated with rhinitis and encephalitis, in farmed caimans in Colombia have been reported by Villafae et al. (1996), who suspected an unknown virus to be the causative agent. In view of the described symptoms and pathology, this agent might very well be a paramyxovirus (see p. 162). A whitish ocular discharge was seen in an outbreak of mycoplasmosis in captive American alligators (Clippinger et al., 1996) (see also p. 167). Severe outbreaks of exudative conjunctivitis affecting a high percentage of hatchlings or juveniles in a pen and spreading rapidly to other pens, occur frequently on Nile crocodile farms in South Africa and are caused by Chlamydia sp. (Huchzermeyer et al., 1994a) (see also p. 167). The condition referred to as ophthalmia by Foggin (1987, 1992a) may, in fact, also be chlamydial conjunctivitis. Some outbreaks of this eye condition appear to have been triggered by outbreaks of crocodile pox (Foggin, 1992a) (see also p. 158). The case of highly contagious keratoconjunctivitis described by Youngprapakorn et al. (1994) may also have been due to chlamydial infection.

Fig. 7.4. One-sided exudative conjunctivitis in a juvenile captive American alligator.

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Treatment In individual cases the brinous exudate may have to be removed from behind the eyelids. After this an antibacterial eye ointment can be administered. In addition, chloramphenicol or another antibiotic can be injected subcutaneously (sc) into the eyelid (Foggin, 1987). Outbreaks of chlamydial conjunctivitis are treated with tetracycline, 1.5 g active ingredient per kg in the feed for 10 days (see Table 2.13). This treatment should be accompanied by thorough cleaning and disinfection of the pens, including spraying the crocodiles with a disinfectant such as F10 (Health and Hygiene, South Africa) at a dilution of 1:250.

Eye injuries Eye injuries can be caused during handling and ghting and may easily become infected. In farmed American alligators several such injuries have been observed, including corneal perforation, uveitis, cataract (see above) and phthisis bulbi (Millichamp et al., 1983). A supercial scratch on the cornea may cause partial opacication (Fig. 7.5), which will disappear once the scratch has healed. Destruction and enucleation of eyes due to injury have been reported from Orinoco crocodiles (Boede, 2000).

Periocular abscess Opacication of the third eyelid Opacication of the third eyelid has been observed in aged captive American alligators, but the nature of the deposit was not determined (Millichamp et al., 1983). Cataract Cataract, the opacication of the lens of the eye, has been observed in farmed American alligators, probably caused by trauma and infection, as well as in an American crocodile (Millichamp et al., 1983). Chorioretinitis Adult captive American alligators in a roadside show were found to have chorioretinitis, with areas of depigmentation and pigment clumping within the tapetal fundus (Millichamp et al., 1983). Ophthalmia A periocular abscess was found in one of the American alligators autopsied during an outbreak of mycoplasmosis (Clippinger et al., 1996) (see also p. 167).

Blindness Occasionally crocodiles are blind from birth (see p. 152). In farming and captive situations blind crocodiles can cope quite well, helped by their acute senses of smell and hearing. Blind Nile crocodiles often are distinguished by a lighter skin colour than that of their pen mates. Cases of congenital glaucoma, with enlarged and protruding eyes and almost complete blindness, occurred in the progeny of a pair of captive African dwarf crocodiles (Fig. 7.6) (authors case). Blindness can also be caused by eye injuries (see above) and temporarily by the brinous exudate produced in cases of conjunctivitis (see above).

Diseases of the Digestive System


The cases and outbreaks of ophthalmia described by Foggin (1987, 1992a) were probably exudative (chlamydial?) conjunctivitis (see above). A case of panophthalmitis, with the infection extending into the eye from a retrobulbar abscess, was reported by Youngprapakorn et al. (1994). Tooth abnormalities Toothlessness Crocodiles replace their teeth regularly (see p. 13). Teeth broken off in ghts will therefore regrow eventually. However, toothless

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Fig. 7.5. Partial opacity of the cornea of a captive Nile crocodile, probably due to a supercial scratch (photograph M. Gansuana).

Fig. 7.6. The bulging cornea of the right eye in a captive-bred African dwarf crocodile with congenital glaucoma.

crocodiles are found or seen occasionally. In old crocodiles this may be due to accumulated damage to the alveoli. Fracturing of a tooth during ghting, or ripping on a prey item, may damage the dental lamina (Erickson, 1996b). The affected alveoli may become permanently edentulous, and, dur-

ing a long life, toothlessness may affect increasingly more alveoli in some individuals. Some such toothless alveoli may become calcied (Hall, 1985). On a Nile crocodile farm where adult breeding crocodiles were dying from stress septicaemia, after having been transferred

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during winter to a new breeding dam (see p. 228), several specimens were seen to have no, or only very small teeth (Fig. 7.7) (authors case). The cause of this condition could not be determined. There is a possibility that in this case there was no permanent damage and that, instead, the teeth were in the process of regrowing. An adult captive mugger, which lost a piece of maxillary bone including parts of ve alveoli and one tooth, regenerated the bone, including the alveoli and the missing tooth (Brazaitis, 1981). Poor mineralization Poor dental mineralization, or a complete lack of mineralization of the teeth, is seen in cases of nutritional osteomalacia (see p. 211). The condition has been dubbed glassy teeth (Huchzermeyer, 1986). In older juveniles, and even in adults, poor mineralization of the teeth is seen from time to time without associated clinical problems, although the presence of osteoporosis in such cases has recently been conrmed (authors cases). The teeth are not completely glassy, but rather opaquely diaphanous (see Fig. 6.9). The underlying cause has not yet been determined. It appeared that the affected animals had received adequate supplies of calcium in their diet. A Ca:P imbalance in the nutrition is a more likely cause.

Protruding incisors Occasionally the long incisors penetrate through the premaxilla and protrude through false nostrils (Fig. 1.21) (see also p. 153). This condition has been seen by myself in captive Crocodylus palustris and Crocodylus niloticus, and appears to be quite common in wild C. johnsoni (Webb and Manolis, 1983). Horizontal orientation A horizontal, sideways, orientation of the teeth is seen in juvenile crocodiles after they have recovered from nutritional osteomalacia (Fig. 6.3) (see p. 211). After the diet has been corrected, the jawbones harden but the teeth remain in their sideways position. In a captive and farmed situation they are able to cope with these non-functional teeth. For congenital defects of dentition see p. 152.

Gingivitis stomatitis Bite-wound gingivitis Cases of gingivitis, sometimes spreading further into the oral cavity (stomatitis), are caused by ghting injuries which become infected (Fig. 6.11). The infection involves a

Fig. 7.7. Lack of fully grown teeth in an adult farmed Nile crocodile.

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variety of bacterial and fungal agents and antibacterial treatment usually does not help to clear the condition, particularly when the antibiotic is given in the ration, as the affected animals may be anorexic. In these cases, injection of vitamin C as well as supplementation of the ration with the same vitamin has cleared up the condition very rapidly (Huchzermeyer and Huchzermeyer, 2001) (see also p. 218). The recommended treatment consists of injecting the badly affected animals individually twice at 48-h intervals with 50 mg ascorbic acid intramuscularly (im), while at the same time supplementing the wet ration with ascorbic acid, 1 g kg 1 continuously. In addition, the pens should be cleaned and disinfected thoroughly. The crocodiles in the affected pens can also be sprayed with a well-tolerated disinfectant, such as F10 (Health and Hygiene, South Africa) at a dilution of 1:250. Greasy gingivitis Gingivitis can also be caused in a fashion similar to greasy skin (see p. 243) by the accumulation of fat and protein from the wet ration, causing dark deposits between the teeth. These deposits are then colonized by bacteria and fungi, which attack the underlying gingival and oral mucosa, causing the affected hatchlings to become anorexic. The treatment is the same as for bite-wound gingivitis (see above). Pox The crusty lesions of caiman, as well as crocodile, pox can be found in the oral cavity, either on the gingivae or on the palate (see pp. 157 and 158). Pox lesions on the gingivae are prone to become infected secondarily by bacteria and fungi. The treatment is the same as that recommended for bite-wound gingivitis. Ulcerative stomatitis A proliferative ulcerative haemorrhagic stomatitis affecting the tongue contained Gram-negative bacteria in the granulomas (Youngprapakorn et al., 1994). Such a lesion

could be the sequel to an injury produced by the sharp point of a bone fragment. Glossitis An inammation of the dorsal surface of the tongue was seen in some of the cases of chronic stress dermatitis described by Huchzermeyer and Penrith (1992) (see pp. 237 and 241). Hyperkeratosis of the oral mucosa Anorexic animals, or animals suffering from septicaemia (see p. 228), often have large areas of the oral mucosa, both tongue and palate, covered with a brownish layer (Fig. 7.8) which, on microscopical examination, is due to hyperkeratosis of the oral mucosa. This is probably caused by latent vitamin deciencies, and cannot be treated unless the underlying condition has been diagnosed and treated. Oral mycobacterial abscesses Mycobacterial abscesses, species undetermined, were seen in the caudal part of the oral cavity, on the tongue and on the gular valve, in a juvenile captive Chinese alligator (Blahak, 1998) (see also p. 170).

Inammation of the gular valve The gular valve serves to separate the oral cavity from the upper respiratory tract (see p. 11) and normally remains tightly closed except during swallowing, yawning and some of the vocalizations. It does not contain any tonsils or tonsil-like tissue. However, an inammation of both velums (aps) of the gular valve, with moderate lymphocytic and round cell inltration, is seen occasionally in juvenile farmed Nile crocodiles (Huchzermeyer and Penrith, 1992) (Fig. 7.9). At the time, the authors speculated that lymphatic cells normally present in the aps of the valve might serve a tonsil-like function. However, the rst case in the report was from a specimen that had been trans-

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Fig. 7.8. Hyperkeratosis of the palate in a juvenile farmed Nile crocodile.

Fig. 7.9. Inammation of the dorsal ap of the gular valve in a juvenile farmed Nile crocodile.

ported a long distance overland, and therefore one might also speculate that the inammation could have been caused by mucosal irritation due to dehydration during the prolonged forced stay out of water. Cases seen subsequently, single deaths, may again have been ailing animals that had also stayed out of the water for a long time, as is common in stressed and anorexic crocodiles (see pp. 278, 282 and 289).

True tonsillar tissue has recently been identied in the roof of the pharynx in Nile crocodiles (Putterill and Soley, 2001) (see p. 24).

Gastric ulcers Gastric ulcers in crocodiles appear to be caused by stress (see p. 278). Many cases

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were seen in juvenile Nile crocodiles associated with chronic stress dermatitis (Huchzermeyer and Penrith, 1992) (see p. 237) as well as in wild-caught Osteolaemus tetraspis after prolonged transport (Huchzermeyer and Agnagna, 1994). Usually, the ulcers are small, with diameters of 24 mm, and are spread throughout the entire surface, or they are concentrated in the pyloric area and the duodenal pouch (Figs 7.10 and 7.11). However, larger ulcers have also been observed. Ulcers infested by ascaridoid nematodes (p. 192) are larger, with diameters up to 10 mm and more (Fig. 5.39). A striking feature accompanying the ulcers is a severe polyarteritis (see p. 269), which is suggestive of a severe autoimmune reaction (Fig. 7.12) (Huchzermeyer and Penrith, 1992; Huchzermeyer and Agnagna, 1994). Gastric ulcers with a diameter of 0.30.7 cm were seen in a captive African dwarf crocodile suffering from septicaemia and arthritis (Heard et al., 1988). Gastric ulcers were found frequently in slow-growing farmed spectacled caimans (Villafae et al., 1996). Very small gastric ulcers lled with brinous exudate and containing bacterial nests were described by Youngprapakorn et al. (1994) as bacterial gastritis.

In the presence of ascaridoids, the parasites will attach to the ulcerated surface and even penetrate into the mucosa (see Fig. 5.40), aggravating the condition (Ladds and Sims, 1990; Foggin, 1992a; Buenviaje et al., 1994; Huchzermeyer and Agnagna, 1994; Ladds et al., 1995) (see also p. 192). Although the gastric ascaridoids colonize the ulcers opportunistically, they do not appear to cause them. It is therefore most likely that all stomach ulcers are stress related, as no other primary pathogens have been found in association with the ulcers. The fungus Mucor circinelloides was isolated from gastric ulcers of a captive crocodilian (Jones, 1978) (see pp. 176 and 179).

Bloating Overeating may be the cause of bloating. Affected crocodiles die suddenly, and their stomach is found to be lled with large pieces of meat (Fig. 7.13). This condition is thought to be caused when hungry animals ingest excessive amounts of insufciently cut meat. Bacterial decomposition continues in the stomach before the gastric acid has been able to penetrate the meat. Gas and bacterial

Fig. 7.10. Small brin-covered ulcers in the stomach of a juvenile farmed Nile crocodile.

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Fig. 7.11. Ulcers of different sizes in the gastric mucosa of a juvenile farmed Nile crocodile.

Fig. 7.12. Arteritis found in association with ulcerative gastritis.

toxins are believed to be responsible for the death (Foggin, 1992a).

Gastroenteritis A case of stress-related gastroenteritis in an adult wild-caught C. palustris was reported by Sinha et al. (1987). The animal became list-

less and anorexic, had an offensive smell from the opened mouth and regurgitated when force-fed with pieces of meat and sh. Proteus rettgeri was isolated from the faeces (see p. 174). Treatment of the condition consisted of: Twice-daily dosing for 5 days with glucoglycelect (sodium chloride, 11.4 g; calcium gluconate, 2.2 g; magnesium sulphate,

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Fig. 7.13. Nile crocodile hatchling which died after having consumed a large meal.

0.61 g; potassium dihydrogen phosphate, 8.68 g; glycine, 21.2 g; and dextrose, 55.67 g), two tablespoons in 250 ml water. Daily dosing for 8 days with vinegar 60 ml. Daily dosing for 8 days with tetracycline 500 mg in 1 l cows milk after bacteriology results became available. Daily dosing for another fortnight with 1 l cows milk with 30 ml vitamin B complex syrup. Continuation for another fortnight of daily dosing with 1 l cows milk. Continuation of daily dosing for another fortnight with meat soup.

After this the animal started eating by itself. Gastric foreign bodies Foreign bodies may be swallowed accidentally or may be part of the food. In a survey of stomach contents of wild American alligators, the following non-food items were found: shotgun shells, dog tags, sinkers, buckshot, shing line, gastroliths (see also p. 36), pieces of wood and coal, nuts and steel nails (Hazen et al., 1978). A wild-caught African dwarf crocodile in poor condition had its stomach distended with large wing feathers (Fig. 7.14) (Huchzermeyer and Agnagna, 1994). Trichobezoars caused gas-

tric blockage in Mexican crocodile hatchlings that had been fed rats. The hatchlings stopped growing, became thin and showed torticollis. A change of diet to minced chicken and sh led to a recovery of the hatchlings (Sigler, 1996). In many cases the animals appear to be unable to regurgitate the unwanted matter. Sharp or pointed objects may penetrate the stomach wall and can damage other internal organs. However, infection is often contained by the inammatory process typical for crocodiles, in the form of briscess formation (see p. 46). A wooden toothpick swallowed by an adult captive American alligator penetrated the stomach wall and caused a subserosal granuloma (Russell and Herman, 1970). Wire mesh, used to block the drain pipes in the rearing pens on a crocodile farm in South Africa, was eaten by a number of juvenile Nile crocodiles (Friedland, 1986). In several of the animals the pieces of wire penetrated the stomach wall and caused localized peritonitis, and in one case severe liver damage. In captive crocodiles the ingestion of foreign bodies may perhaps not be accidental but caused by disturbed behaviour (see p. 289). The surgical removal of gastric foreign bodies, gastrotomy, is described in Chapter 2 (p. 94). Gastric foreign bodies have also been suspected to have caused cirrhosis of the liver (see p. 261).

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Fig. 7.14. Stomach that had been distended by large feathers; wild-caught African dwarf crocodile.

Sticks are embedded into sh or frogs used as bait and tied by a length of string to a tree at the edge of the water. When the bait is swallowed by a crocodile the string often breaks, allowing the crocodile to escape. However the stick remains in the stomach and often works its way through the stomach wall and into other organs (Figs 7.15 and 7.16). This is one of the common hunting methods used to catch African dwarf croco-

diles in the Congo Republic, and several such cases were found in our material (Agnagna et al., 1996).

Enteritis The multifactorial aspect of enteritis has been discussed in Chapter 6 (p. 226). Here, the emphasis is on the different forms and

Fig. 7.15. Bait stick attached to the outside of the stomach of a wild-caught African dwarf crocodile, after having penetrated the stomach wall.

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Fig. 7.16. Section of the stomach wall of a wild-caught African dwarf crocodile with a subserosal granuloma around a remaining piece of a bait stick.

manifestations of enteritis which have been seen in crocodiles. These different forms depend on the pathogenic agent causing the enteritis and on the inammatory response elicited by the infection. Necrotic Severe necrotic and exudative enteritis is seen in cases of coccidiosis (see p. 183), as well as in cases of adenovirus infection (Foggin, 1992a) (see p. 160), and in both instances is probably caused by secondary bacterial infection of the mucosal lesions caused by the primary agents. In these cases, the necrosis penetrates deep into the muscular layer of the intestine, while the exudate lls the intestinal lumen, causing occlusion of the intestine (see also p. 258). Because of the occlusion there is no possibility of delivering a drug to the affected parts of the intestine. Any treatment must be aimed at saving the less-affected animals (see p. 183). Exudative Bacterial enteritis, in hatchlings caused frequently by Salmonella serovars and pathogenic serotypes of Escherichia coli (see p. 145, 164 and 174), usually manifests itself in the form of a severe exudative enteritis with dis-

tension of the intestine by the brinous mass (Plate 20). With a blocked intestine, the hatchlings are unable to digest and lose weight, while the abdomen becomes distended with the brinous material accumulating in the intestine (see Fig. 4.7). The affected animals die slowly of starvation. Once the intestine is blocked by the brinous exudate, there is no possibility of treating the affected animals. In older juveniles, the exudate does not necessarily cause an intestinal occlusion, and such animals pass pieces and strands of brin in their faeces. On occasion these have been mistaken for tapeworm segments. Note that crocodiles do not have tapeworms (see p. 203). Ulcerative A case of ulcerative enteritis was found associated with an encephalitis of suspected viral origin (authors case) (see p. 266). Nodular A form of chronic enteritis characterized by severe lymphoproliferation in the form of distinct nodules was seen several times in Nile crocodiles (authors cases) (Figs 7.17 and 7.18). However, we were not able to determine the cause of this condition.

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Fig. 7.17. Nodular enteritis in a Nile crocodile hatchling.

Fig. 7.18. Section of the intestine of a Nile crocodile hatchling with nodular enteritis: lymphoproliferative lesion penetrating through the intestinal muscularis.

Haemorrhagic Damage to the intestinal epithelium and the capillaries can, in very acute cases of enteritis, lead to haemorrhage into the intestine. In crocodiles this is relatively rare, as the exudative response usually prevents any bleeding. A case of haemorrhagic enteritis was seen in juvenile farmed Nile crocodiles in South Africa, associated with a clostridial septicaemia (Plate 21) (authors case). Coronavirus-like particles were found in the

faeces of a healthy pen mate of the affected crocodiles (see p. 163). A haemorrhagic enteritis in a 2-month-old crocodile hatchling with non-resorbed yolk-sac was described by Youngprapakorn et al. (1994). Colitis A brinonecrotic colitis has been seen repeatedly in juvenile farmed Nile crocodiles in South Africa (authors cases). The colon was distended (Fig. 7.19) and the mucosa covered

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Fig. 7.19. Distended rectum in a juvenile Nile crocodile with colitis.

by a brinous exudate (Fig. 7.20). The cause could not be determined. It is to be noted that in chronic cases the causative agent may no longer be present when death occurs. A case of amoebic colitis occurred in a crocodile (species not given), when snakes in the same collection suffered from an outbreak of amoebiasis (Ippen, 1965) (see p. 192).

Intestinal occlusion Intestinal occlusion may be congenital (Youngprapakorn et al., 1994) (see also p. 155), due to exudative enteritis (see

above), injury or torsio. A penetrating bite wound in an adult captive Nile crocodile caused the closure of the ileum, with the slow accumulation of faecal masses craniad of the lesion (Fig. 7.21). The animal was seen losing condition while the abdomen became distended, and in the end the animal had to be euthanized (authors case). Several cases of intestinal occlusion are shown by Youngprapakorn et al. (1994) under the name of diphtheritic mass obstruction. The onion peel architecture is typical of the successive layers of brin deposited in cases of chronic exudative inammation (see p. 46).

Fig. 7.20. Colitis: the mucosal surface of the colon is covered by a layer of brinous exudate.

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Fig. 7.21. Large faecal mass in the ileum of an adult captive Nile crocodile craniad of the healed bite wound that caused the intestinal occlusion (photograph H. Lagasse).

A case of torsio intestinalis was seen in a Nile crocodile hatchling (authors case). The severe congestion normally seen in avian and mammalian intestinal strangulation was not present in this case (Fig. 7.22).

lation of lymphocytes in the tissue (Fig. 7.24) (authors cases). In some cases of adenovirus infection, intranuclear inclusion bodies are found in the acinar cells (Foggin, 1992a) (see also p. 160, Fig. 5.5). Pancreatic thrombosis A case of pancreatic thrombosis was seen in a crocodile with haemorrhagic enteritis caused by Clostridium perfringens (authors case) (see also pp. 172 and 257). Involution of the pancreas Chronically ailing juvenile Nile crocodiles were found to suffer from an involution of the pancreas, which appeared to be replaced by fat tissue between the duodenal loops (Fig. 7.25) (authors cases). The cause of this condition remained undetermined.

Cloacitis Overfed American alligators tended to protrude the cloaca by as much as 5 cm. If the animals spent much time on rough concrete, the protruded cloaca received abrasions and became inamed. Keeping the animals in the water and fasting them led to an improvement of the condition within a few days (Coulson et al., 1973). Histopathologically, a cloacitis was found in one of the wild-caught and severely stressed African dwarf crocodiles sampled on markets in the Congo Republic (Fig. 7.23) (authors case). Linear ulcerations of the cloaca lled with yellow keratinized debris have been described from cases of steatitis (Wallach, 1971) (see p. 219).

Hepatitis Adenoviral hepatitis

Pancreatitis Pancreatitis sometimes occurs as part of a septicaemia, occasionally seen as an accumu-

Hepatitis is a common manifestation of adenovirus infection in Nile crocodiles (see p. 160). The liver is swollen and pale and the bile of light brown colour. Adenoviral inclu-

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Fig. 7.22. Juvenile Nile crocodile with torsio of the intestinal loops; the strangled loops are lled with gas.

Fig. 7.23. Section of the cloaca of a wild-caught African dwarf crocodile with cloacitis.

sion bodies are found in the hepatocytes. Chronic changes include brosis of the portal tracts and bile duct hyperplasia (Foggin, 1992a). Chlamydial hepatitis Chlamydial hepatitis is the acute form of crocodile chlamydiosis (see p. 167). The liver is pale and enlarged. The histopathological lesions are severe portal to diffuse lymphoplasmocytic hepatitis, with congestion, mild

bile duct proliferation, vacuolar degeneration of hepatocytes and multifocal to coalescing necrosis. Chlamydial colonies are present in many hepatocytes (Huchzermeyer et al., 1994a). Non-specic bacterial hepatitis Bacterial complex presence nests to hepatitis is part of the septicaemia (see p. 228). It can range from the of small granulomas with bacterial multifocal and conuent necrosis

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Fig. 7.24. Lymphocytic inltration in the pancreas of a farmed juvenile Nile crocodile.

Fig. 7.25. Involution of the pancreas in a juvenile Nile crocodile; large portions of the pancreas between the duodenal loops are replaced by fat tissue.

(Villafae et al., 1996). A chronic hepatitis with cirrhosis in a captive American alligator was interpreted as being of toxic origin because of the presence of coins in the stomach (Will, 1975). However, crocodiles have been found to tolerate very high metal levels (see p. 221).

A fatty degeneration of the liver is seen in starving crocodile hatchlings, part of the runting syndrome (see p. 234). Fatty degeneration with mild brosis and bile duct proliferation was seen in juvenile and adult farmed caimans and interpreted as probably caused by mycotoxins (see p. 236) or vitamin B1 deciency (see p. 217) (Villafae et al., 1996).

Degeneration of the liver Liver parasites Degeneration of the liver can be caused by toxic and nutritional factors. It can also occur due to infection as part of the inammatory process (see above). Rhabditid nematodes were found in the liver of a captive African dwarf crocodile from a South African zoo (Huchzermeyer et al.,

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1993) (see p. 198). Coccidial stages are found in the liver in cases of generalized coccidiosis (see p. 183) with severe inammatory reaction, and schizonts of the blood parasite Hepatozoon are also found in the liver (see p. 188), but without any tissue reaction.

Cholecystitis Infections of the gall bladder usually ascend from the intestine. Exudative cholecystitis caused by coccidia was described by Foggin (1992a) (see also p. 183). An exudative and haemorrhagic bacterial cholecystitis was seen in an adult crocodile that had suffered from anorexia, weakness and emaciation (Youngprapakorn et al., 1994). Similar cases have been seen in juvenile farmed Nile crocodiles (authors cases), including one with a severely distended bile duct due to an exudative inammation (Fig. 7.26). An apparently common haemorrhagic syndrome has been described by Youngprapakorn et al. (1994), in which haemorrhages occur into the inamed gall bladder. The affected 34-month-old farmed crocodiles become anorexic, anaemic and emaciated, and die. The liver has a pale grey colour and the blood is very watery.

Inammation and haemorrhage are found in the gall bladder. Small emphysema lesions are seen in the lungs. The cause of this disease has not yet been determined. Choleliths gall bladder stones probably form in the altered environment caused by a mild infection. Such stones have been found in farmed crocodiles (Youngprapakorn et al., 1994) and in an adult captive American alligator (Clippinger et al., 1996). Two functioning gall bladders were found in a farmed Nile crocodile hatchling (authors case) (see p. 155).

Steatothecitis The inammation of the abdominal fat body steatotheca occurs in cases of septicaemia (see p. 228) (Fig. 7.27) and in cases of pansteatitis, fat necrosis (see p. 219). In the cases of chlamydiosis (see p. 167) described by Huchzermeyer et al. (1994a), multiple small foci of necrosis were seen in the fat body. In some cases of generalized mycobacteriosis (see p. 170) in juvenile farmed Nile crocodiles, granulomas containing acid-fast rods were found in the fat body (see Fig. 5.13) (authors cases).

Fig. 7.26. Choleangitis in a juvenile farmed Nile crocodile; the distended bile duct lies across the duodenal loops; part of the liver has been removed.

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Fig. 7.27. Steatothecitis; note the dark colour of the fat body and the small necrotic foci.

Injuries to the fat body can occur from penetrating gastric foreign bodies (Fig. 7.28) (see p. 254). A two-lobed fat body was found in a juvenile farmed Nile crocodile (authors case) (see p. 155).

depends on the absolute freshness of the specimens, as post-mortem changes mimic many of the degenerative changes. This may explain the sparseness of reports on kidney affections in the veterinary crocodile literature.

Diseases of the Urogenital System


Pyelonephritis Infections of the organs of the urogenital system can either originate from septicaemias (see p. 228) or ascend from the cloaca. The exact diagnosis of many kidney conditions A one-sided pyelonephritis caused the enlargement of the affected kidney, with exudate lling the ducts, which were lined by an

Fig. 7.28. Fat body of a wild-caught African dwarf crocodile pierced by a bait stick which had migrated out of the stomach.

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epithelium showing squamous metaplasia (see also pp. 216 and 230) and a granulomatous response (Ladds et al., 1995). In the renal tissue there was a diffuse chronic interstitial nephritis with foci of intense inltration by granulocytes. Most likely an ascending infection had been facilitated by a latent vitamin A deciency (see p. 216). In farmed Nile crocodiles, a gross enlargement of the kidneys was seen in cases of pyelonephritis (Huchzermeyer, 1994). Pyelonephritis as a result of uke infestation (see pp. 200 and 265) was seen in juvenile farmed crocodiles in Papua New Guinea (Ladds and Sims, 1990).

epicardium, a well as throughout the musculature. This occurs when, for one or other reason, the kidneys cannot excrete the urates in the urine. This may, or may not, be associated with histopathological lesions in the kidneys. For a detailed discussion of the multifactorial aspect of gout in crocodiles see p. 230. Dehydration is one of the predisposing factors, and in these cases a hyaline droplet degeneration of the tubular epithelial cells is seen (Foggin, 1992a).

Vitamin A deciency Vitamin A deciency (see p. 216) causes squamous metaplasia of the epithelium of the collecting ducts of the kidneys of crocodiles, and this may predispose the kidneys to ascending infections (see above) and to gout (see above and p. 230) (Foggin, 1992a; Buenviaje et al., 1994).

Kidney aplasia Occasionally only one kidney develops, and in such cases the remaining kidney is larger than normal (Huchzermeyer, 1994). The enlargement serves to compensate for the missing kidney.

Hyaline degeneration Gout Gout is caused by the deposition of urate crystals in the kidneys, in the joints of the limbs, on serosal surfaces, particularly the peri- and Hyaline degeneration of the kidneys (Fig. 7.29) was found in an adult farmed Nile crocodile that had been translocated to a new breeding enclosure during winter and had

Fig. 7.29. Macroscopically visible hyaline degeneration of parts of the kidney (arrow) of an adult farmed Nile crocodile; the still functioning renal folds are dark.

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died from stress septicaemia (p. 228). In green iguanas the macroscopically visible hyaline degeneration has been linked to vitamin D toxicity, hypervitaminosis D (Wallach, 1966) (see also p. 225).

Kidney parasites Two kidney ukes are known from crocodiles, Deurithrema gingae and Renivermis crocodyli (Blair, 1985; Blair et al., 1989) (see also p. 260), both from C. porosus, but the former also from C. novaeguineae (Ladds and Sims, 1990). These latter authors also found numerous blood ukes, probably Griphobilharzia amoena (Platt et al., 1991) (see also p. 200) in the parenchyma of the kidneys, some encapsulated and surrounded by severe tissue reaction. In addition, Exotidendrium sp. has been found in the kidneys of Nile crocodiles (Foggin, 1992a). Unidentied nematodes, 5 mm long, were found in the severely swollen kidneys of a juvenile captive gharial (Maskey et al., 1998).

den warm spell after a prolonged cool period, can play a role in triggering such an event. A disturbed calcium metabolism after the depletion of Ca reserves for the production of the eggshells could also be considered. Malformation of the cloaca in a tailless crocodile has been cited as another cause (Youngprapakorn et al., 1994). If such a case is seen early, before any damage has occurred to the everted uterus, repositioning of the uterus may be attempted. For this the crocodile is immobilized (see p. 70) and the everted uterus washed to remove any sand particles, best in a mild disinfectant solution. After cleaning, the size of the, often swollen, uterus is reduced by either gently massaging it with ice cubes, by sprinkling tetracycline powder on it, or gently dabbing it with a dimethylsulphoxide (DMSO) solution. Once the uterus has shrunken to a smaller size, it can be replaced in its correct position via the cloaca. Note that there are two uteri and that each one has to be replaced into its own side.

Infection of oviduct and uterus Infection and inammation of the oviduct, oophoritis, and of the uterus, endometritis, can be caused by ascending infections originating from intestine or cloaca, but also originate from penetrating bite wounds. If, for some reason, hormonal or metabolic, not all eggs are laid, the eggs remaining in the uterus may act as foreign bodies and also elicit an inammatory response. In all cases there is an exudative response (see p. 46), the brin often deposited in successive layers, onion-peel fashion, frequently forming large masses. Usually there are no clinical signs and the condition is diagnosed on post-mortem examination only.

Ectopic eggs Mature follicles or whole eggs sometimes nd their way into the peritoneal cavity, where they cause a foreign-body peritonitis (egg peritonitis), often with a pronounced exudative response, particularly if accompanied by a bacterial infection. A case of chronic diffuse proliferative serositis, caused by the presence of egg yolk in the abdominal cavity, was found in a wild American alligator (McDonald and Taylor, 1988). Mature follicles can fall into the peritoneal cavity when, during ovulation, the infundibulum of the oviduct fails to catch the follicle as it comes loose from the ovary. A severe disturbance at the moment of ovulation, as caused by ghting or capture, can cause this failure. Whole eggs with shell leave the uterus either through a rupture (Youngprapakorn et al., 1994), or they are moved by antiperistalsis back up the oviduct and out through the infundibulum. A severe disturbance, probably also ghting, may cause this antiperistalsis. The rupture may be

Prolapse of the uterus Prolapse of the uterus can occur during egg laying, due to excessive straining. It is possible that unusual weather conditions, a sud-

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due to prolonged presence of the eggs in the uterus after the female, for some reason, failed to lay her eggs. In many of these cases the affected crocodile may live and appear normal for a long time after the event, but eventually will become ill and die.

delayed. Delayed clotting was found in domestic laying hens during routine blood sampling, when the samples were taken in the morning at the time when the shell was being deposited (authors unpublished observation).

Cystic gonads Orchitis A case of necro-granulomatous orchitis was found in an adult farmed Nile crocodile that had died from septicaemia (authors case) (see also p. 228). Occasionally, cysts have been found incidentally in the immature gonads of juvenile Nile crocodiles (Fig. 7.30). The cysts are probably due to harmless malformations (authors cases).

Impaired penis development Juvenile male American alligators living in Lake Apopka, Florida, showed a 24% reduction in penis size when compared with animals of the same body length from another lake in Florida. This reduction was caused by endocrine disruption due to exposure to elevated concentrations of the DDT breakdown product p,p-DDE, which is known for its anti-androgenic properties (Guillette et al., 1996) (see also p. 223).

Diseases of the Nervous System


Some of the conditions dealt with in this section are not nervous disorders in a strict sense, but rather they mimic nervous problems. This grouping by symptoms has been done to facilitate diagnosis.

Encephalitis Encephalitis can be caused by bacteria as the sequel of a septicaemia (see p. 228) or by viral infections. A case of granulomatous encephalitis, probably of parasitic origin, was presented by Youngprapakorn et al. (1994). Cases of presumably viral encephalitis with lymphocytic perivascular cufng were diagnosed in farmed crocodiles in Papua New Guinea (Ladds and Sims, 1990). A lymphocytic and plasmocytic encephalitis in very young juvenile farmed caimans occurred in association with conjunctivitis and rhinitis (Villafae et al., 1996) (see also pp. 245 and 270). It is suggested that a paramyxovirus might be involved in these cases (see p. 162). This needs further investigation. My own cases in farmed Nile crocodiles were as follows. A small juvenile in good nutritional state and without noticeable clinical symptoms. Brain lesions included perivascular cufng, glial proliferation, vacuolization of the nerve cells in the cerebel-

Ovarian haemorrhage Before ovulation there is a strong supply of blood to the ovum, needed for the deposition of nutrients in the yolk. At the time of ovulation the blood supply to the ovum needs to be cut off, otherwise haemorrhage may occur. If there is a failure of the blood clotting system, due to low calcium levels or lack of vitamin K, for example, the haemorrhage may become fatal. This is believed to have occurred with a captive female mugger, which was found dead with a massive internal haemorrhage. The ovulated eggs had reached the shellgland portion of the oviduct (uterus), but only a thin layer of shell had been deposited (Whitaker and Huchzermeyer, 2000). The calcium demand for the production of the shells must have reduced the calcium level in the blood to such an extent that coagulation was

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Fig. 7.30. Testicular cyst in a juvenile Nile crocodile.

lum and demyelinization. This case was associated with small ulcers in the ileum (see p. 255). The second case involved a crocodile of length 1.2 m in good nutritional state with petechiae in the brain (Fig. 7.31) and foci of lymphocytic inltration. Symptoms of encephalitis may vary with the location of the lesions in the brain. Excitability, incoordination, opisthotonus, convulsions and weakness were seen by Youngprapakorn et al. (1994). Other symptoms may be circular movements and inability to swim in an upright position. Meningitis Outbreaks of meningitis occurred in farmed 4-month-old C. porosus. The outbreaks were associated with septicaemia caused by Providentia rettgeri (Ladds et al., 1996) (see also pp. 172 and 228). Meningitis was also present in cases of experimental infection of American alligators with Mycoplasma alligatoris (Brown et al., 2001b) (see also p. 167).

Encephalomalacia Villafae et al. (1996) describe a condition with nervous symptoms in juvenile and adult farmed caimans, leading to episodes of mortality, in which they nd encephalomalacia, but with perivascular cufng (see above), and also fatty degeneration of the liver. The authors suspect either mycotoxicosis (see p. 226) or thiamin deciency (see p. 217). In poultry, encephalomalacia is caused by rancid sh oil in a syndrome similar to fat necrosis in crocodiles (see p. 219), but the perivascular cufng could be indicative of a viral infection.

Posterior paralysis Fractures of the spine are caused by violent spasms in calcium-decient juvenile farmed crocodiles fed red meat exclusively (see p. 211) (Figs 6.4 and 6.5). Affected animals have paralysed hind limbs. There is no treatment.

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Fig. 7.31. Petechiae on the cut surface of the brain of a juvenile farmed Nile crocodile with encephalitis.

Star gazing The main symptom of thiamin deciency is star gazing opisthotonus (see p. 217). This occurs mainly in crocodile hatchlings and juveniles fed sh exclusively (Santos et al., 1993). In the case described by Youngprapakorn et al. (1994) there was also a distinct forelimb paralysis.

odiles in Papua New Guinea, with and without granulomatous tissue reaction (Ladds and Sims, 1990). The eosinophilic granulomata found in a crocodile brain by Youngprapakorn et al. (1994) may also have been elicited by parasites.

Diseases of the Circulatory System


Metazoan parasites of blood and blood vessels Griphobilharzia amoena has been found in the blood vessels of Crocodylus johnsoni, C. novaeguineae and C. porosus (Ladds and Sims, 1990; Platt et al., 1991; Ladds et al., 1995) (see also p. 200). The male is 2.5 mm long and contains the smaller female entirely in a gynecophoric chamber. When trapped in the capillaries of internal organs, the parasite can cause localized inammatory reactions. Larvae and nymphae of the pentastome Leiperia cincinnalis are found in the aorta of the Nile crocodile (Rodhain and Vuylsteke, 1932) (see also p. 205), while the adults are found in the trachea and the two bronchi (see p. 271).

Leg weakness Leg weakness is often the rst noticeable symptom in cases of nutritional bone disease (osteomalacia) in crocodile hatchlings fed a red meat diet (see p. 211). This occurs even before deformation of the vertebral column takes place. Often the affected hatchlings can be seen swimming normally, but they can no longer crawl out on to the dry parts of the pen.

Brain parasites Stages of the blood-vessel parasite, Griphobilharzia amoena (see p. 200 and below), have been found in the brain of farmed croc-

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Microlariae, the larvae of larial worms (see p. 197), can be found in blood smears of crocodiles harbouring these parasites (see Fig. 5.44).

Protozoan blood parasites The protozoan blood parasites of crocodiles belong to the genera Hepatozoon (see p. 188), Progarnia (see p. 190) and Trypanosoma (see p. 191). None of these are regarded as pathogenic.

Endocarditis The inammation of the endothelium of the heart, particularly the valves, is caused by non-specic bacterial infections during septicaemia (see p. 228). It interferes with the functioning of the heart, eventually causing death (Youngprapakorn et al., 1994).

of values for the relative mass of the right ventricle (right ventricular mass divided by total ventricular mass) of 0.220.36, with a mean of 0.286. Chronic hypoxia, as in altitude disease, causes a hypertrophy of the right ventricle in certain birds and mammals. However, diving animals appear to be more resistant against hypoxia. Most of the crocodiles examined in the survey had been kept at an altitude of >1200 m above sea level. The mean right ventricular mass of the crocodile hearts was higher than that of normal domestic fowls kept at the same altitude, but there was no case of outright right ventricular hypertrophy in the surveyed group.

Arteritis Severe arteritis with intima proliferation and lymphocytic inltration of the adventitia (Fig. 7.32) was found in association with gastric ulcers (see p. 251) in juvenile farmed Nile crocodiles (Huchzermeyer and Penrith, 1992) and in adult wild-caught African dwarf crocodiles (Huchzermeyer and Agnagna, 1994). The gastric lesions appeared to be stressrelated (see p. 278). The vascular lesions were not limited to the stomach wall, but could be found in various organs and parts of the body, suggesting a severe chronic autoimmune reaction. The mechanisms involved in this syndrome need further investigation.

Pericarditis Pericarditis, epicarditis (both exudative) and myocarditis may be found associated with acute septicaemia (see Plate 11) (Ladds and Sims, 1990) (see pp. 173 and 228). In cases of pericarditis, there may be a considerable accumulation of brinous exudate in the pericardial sac, which may, in fact, strangle the heart. Pericarditis and myocarditis were found in experimental infection of American alligators with Mycoplasma alligatoris (Brown et al., 2001b) (see also p. 167).

Anaemia Anaemia can be caused by severe or chronic bleeding, or by malnutrition. It is also associated either with chronic disease or runting. Haemorrhage can occur through wounds or in the form of a haemorrhagic enteritis (see p. 255). It could also be associated with a vitamin K deciency (see p. 219) or rodenticide poisoning (see p. 224). Youngprapakorn et al. (1994) mention anaemia as one of the symptoms of thiamin deciency (see p. 217). For a detailed discussion of runting see Chapter 6 (p. 234).

Cardiac hypertrophy Enlargement of the heart has been described as one of the lesions associated with thiamin deciency (Youngprapakorn et al., 1994) (see p. 217). Using data from 453 routine post-mortem cases (Nile crocodiles) Huchzermeyer (1994) found a strong correlation between body length and heart mass, and, on a smaller sample (n = 36), a reasonably narrow range

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Fig. 7.32. Arteritis in a juvenile Nile crocodile with ulcerative gastritis.

Splenomegaly A hypertrophy of the spleen is caused by the proliferation of the white pulp when the animal is challenged by certain infectious agents. The crocodile spleen has a very strong brous capsule, which cannot quickly accommodate the increase of spleen tissue. Consequently the spleen tissue breaks through the capsule in the form of buds (Fig. 1.46) (Huchzermeyer, 1994). For an exact measurement of the relative mass of the spleen, the spleen:heart ratio (SHR) should be established by weighing the spleen as well as the ventricles of the heart and dividing spleen mass by ventricular mass (Huchzermeyer, 1994) (see p. 85). Ranges of SHR values from normal crocodiles and crocodiles suffering from various infections are given in Table 2.12. These values were established during post-mortem examinations carried out between January 1991 and December 1993. The very low values at the low end of the ranges are due to the fact that chronic disease causes an involution (shrinking) of the spleen. Normal SHR values lie between 0.3 and 0.5.

nial portion of the septum between the two ventricles of the heart. It is not known how this could have affected its ability to dive (Brockman and Kennedy, 1962).

Diseases of the Respiratory System


Rhinitis A rhinitisconjunctivitisencephalitis syndrome of suspected viral origin occurs in farmed spectacled caimans, 3 months of age and older (Villafae et al., 1996) (see also pp. 162, 245 and 266). A chronic syndrome, chronic stress dermatitis, involving the skin of the head, particularly around the nostrils, a rhinitis in the nostrils, but not involving the deep nasal passages, ulcerative gastritis and severe arteritis, occurs in older juvenile and subadult Nile crocodiles (Huchzermeyer and Penrith, 1992) and appears to be associated with chronic stress (see pp. 237, 241, 251, 269 and 278).

Pharyngitis and rhinopharyngitis Interventricular septal defect A juvenile captive American alligator, approximately 18 months old and apparently clinically normal, had a hole in the craPharyngitis has been seen occasionally in farmed Nile crocodiles in association with septicaemia (see p. 228). The inammation involves the tonsillar tissue in the roof of the pharynx, the dorsal ap of the gular valve

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and sometimes also the glottis (Plates 22 and 23). Pharyngitis has also been found in a captive C. palustris which suffered from granulomatous pneumonia (see below) (Rahman, 2000). A disease referred to as rhinopharyngitis occurs in crocodile hatchlings in Thailand. The affected animals have a runny nose with an accumulation of discharge around the nostrils, as well as a congestion of the roof of the pharynx in the tonsillar area (see p. 11), and severe oedema of the larynx (Youngprapakorn et al., 1994). The cause of this disease has not yet been determined.

dilians (Vargas, 1971, 1975; Riley et al., 1990). As it is difcult to open the nasal passages of an adult crocodile, one can rather try to ush out the parasites by injecting a quantity of water into the nostrils (Vargas, 1971, 1975). Trachea and bronchi The adults of the pentastomid Leiperia cincinnalis are found in the trachea and the two bronchi of the Nile crocodile, rmly attached with one-third of their anterior end burrowed in the tracheal mucosa, and surrounded by a friable substance, probably brinous exudate (Rodhain and Vuylsteke, 1932; Junker et al., 2000) (see also p. 205). Lungs All other pentastomids occur in the lungs (see p. 205), often without eliciting any inammatory response. However, localized foci of inammation may occur in the lungs due to bacterial infection, possibly triggered by stress and/or septicaemia (Ladds and Sims, 1990). Four-week-old American alligator hatchlings fed with infested sh became anorectic, lethargic, dyspnoeic and died. On post-mortem examination they had multifocal haemorrhages in the alveoli and bronchi (Boyce et al., 1984). The parasites themselves are protected from the strong immune response of the host by constantly renewed surface membranes, excreted by the parietal glands and covering all sensitive areas of the pentastomids (Riley et al., 1979). Stages of the blood-vessel parasite Griphobilharzia amoena (see pp. 200 and 268) have been found in the lungs of farmed crocodiles in Papua New Guinea, with and without granulomatous tissue reaction (Ladds and Sims, 1990). In cases of generalized coccidiosis (see p. 183), sporulated oocysts are found in the lungs as well as in other organs (Ladds and Sims, 1990; Foggin, 1992a).

Bronchopneumonia A chronic proliferative bronchopneumonia was found in a juvenile farmed Nile crocodile, which also had ulcerations of the lingual mucosa, chronic hepatitis and interstitial nephritis, all suspected to be manifestations of a chronic septicaemia (authors case) (see also p. 228).

Fungal pneumonia Fungal pneumonia is usually focal or multifocal, with the formation of large granulomas with diameters ranging from <5 mm to 20 mm and more (see Fig. 5.26). Predisposing factors and the species of fungi isolated from such lesions have been discussed in Chapter 5 (p. 178). A case of granulomatous pneumonia was reported from a captive C. palustris (Rahman, 2000).

Mycoplasmosis Pneumonia was seen in cases of mycoplasmosis in farmed Nile crocodiles (Mohan et al., 1995) (see p. 167).

Parasites of the respiratory system Nasal passages and pharynx Pentastomids (see p. 205) of the genus Subtriquetra as well as Sebekia jubini are found in the nasal passages and pharynx of croco-

Adenoviral pneumonia While adenoviral infections (see p. 160) normally affect liver, intestine and pancreas,

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cases of adenoviral pneumonia have also been seen (Foggin, 1992a). The diagnosis is based on detection of the intranuclear inclusion bodies in histopathological sections of the lungs.

Lung emphysema Emphysematous bullae form in the lung when the air passages are obstructed, as in the case of multifocal granulomatous pneumonia in a captive American alligator infected with Fusarium moniliforme (Frelier et al., 1985) (see also pp. 176 and 178), in association with fungal granulomata in farmed Nile crocodiles (see Fig. 5.26) (authors cases) and also in farmed crocodile hatchlings in Thailand with mucus obstructing the trachea in cases of cholecystitis (Youngprapakorn et al., 1994) (see also p. 262).

Foreign-body pneumonia A 4-month-old farmed Nile crocodile hatchling with non-resorbed yolk-sac had, on post-mortem examination, greyish nodules in both lungs. On histopathological examination the lesions were found to be air spaces lled with granular material, probably aspired proteinaceous liquid (authors case).

Diseases of the SkeletalMuscular System


Osteomalacia Lack of calcium and phosphorus in the rations of captive and farmed crocodile hatchlings is the most common cause of osteomalacia, particularly if the hatchlings are fed red meat exclusively. The rst symptom noticed is leg weakness (see p. 268), the affected animals being unable to move on land but capable of swimming. This is followed by deformation of the vertebral

Lung haemorrhage Alveolar and bronchial haemorrhages occurred in young American alligator hatchlings which became infected with pentastomes (see pp. 205 and 271). Occasionally lung haemorrhage has been seen on postmortem examination of juvenile farmed Nile crocodiles, but the cause of the haemorrhage could not be established (Fig. 7.33) (authors cases).

Fig. 7.33. Focal disseminated haemorrhages in the lung of a juvenile Nile crocodile.

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column. Further signs are rubber jaws and glassy teeth (see p. 211). In juvenile crocodiles the teeth may be bent into a horizontal position (see p. 247) and fractures of the vertebral column may cause hind-limb paralysis (see p. 267).

Polydactyly The presence of supernumerary toes on the feet on one side, or on all four feet, is a relatively common birth defect (see p. 151) and usually has no deleterious effect on the functioning of the limbs. Claw abnormalities Sideways bending of the claws on all four feet is probably caused by a birth defect. However, laterally or dorsally curved or malformed individual claws are believed to be due to healed injuries (Webb and Manolis, 1983). Occasionally crocodiles of any species may have one or more white claws. However, all the specimens of Tomistoma schlegelii in the Singapore Zoological Gardens have white claws (Fig. 7.34). If this was caused by any external factors, such as water quality or chemicals in the water, all the other crocodiles in the collection should also have white claws, but this is not so. It is therefore suggested that the false gharials in this collection all derive from the same wild population, which is characterized by this particular trait. However, these crocodiles were obtained from a trader and their origin is unknown (personal communication, P. Martelli, Singapore, 1996).

Osteoporosis Many cases of mild to moderate osteoporosis occur on crocodile farms in South Africa (authors cases) (see p. 211). The function of the limbs does not appear to be affected, and for that reason the farmers do not see this as a problem. The outstanding clinical symptom is poor dental mineralization, diaphanous teeth (see Fig. 6.9), which still remain sharp and functional. The cases occur on farms with on-farm feed mixing. However, the actual causes of this condition have not yet been identied. Three cases of combined brous osteodystrophy, osteochondrosis and osteoporosis in captive adult or subadult Crocodylus intermedius and C. acutus, with luxation of one or more limbs and subsequent articular changes, were described by Blanco (1997). The causes were probably a combination of malnutrition and injuries.

Limb abnormalities Extra limbs The presence of extra limbs is due to birth defects (see p. 151). They always are nonfunctional, but may not interfere with the function of the four normal limbs. Missing limbs Missing limbs may be due to birth defects (see p. 151), to injuries (see p. 284) or to inammatory and necrotic processes, as in a case of digital emphysema (see p. 288). While captive and farmed crocodilians may be able to cope with one or two limbs missing, certain reproductory functions, such as copulation and nesting, may not be possible without the use of the limbs.

Arthritis Arthritis affecting a single joint can be caused by a septic injury (see p. 284). Polyarthritis can be the sequel of a specic infection like mycoplasmosis (see p. 167) or of a non-specic septicaemia (see pp. 173 and 228). There may a visible swelling and an unwillingness, or inability, to move the affected limb(s). Similar signs can also be seen in some forms of gout (see pp. 230 and 264). No successful treatment of arthritis in crocodiles has ever been reported. An attempt to treat a case of septic arthritis in a green sea turtle using antibiotic-impregnated polymethyl methacrylate beads in a local application, in addition to systemic antibiotics, was not successful (Helmick et al., 1999).

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Fig. 7.34. White claws on a false gharial in Singapore Zoological Gardens.

Myositis A case of skeletal muscle myositis was mentioned by Hibberd et al. (1996) in a survey of diseases in farmed juvenile C. porosus, but no further details were given. Debyser and Zwart (1991) isolated the fungus Cephalosporium sp. from small white muscle lesions of a spectacled caiman (see p. 182).

White muscle disease An outbreak of white muscle disease occurred in juvenile farmed Nile crocodiles. The cause was presumed to be a vitamin E and selenium deciency (authors case) (see also p. 219).

in Louisiana (Ash, 1962) (see pp. 197 and 199). Cestode larvae, plerocercoids, were found in the muscle tissue of farmed C. johnsoni kept in earth ponds (Melville, 1988; Millan et al., 1997b) and of a wild-caught African dwarf crocodile slaughtered at a market in the Congo Republic (authors case) (see p. 203). The possible presence of all the muscle parasites should be taken into consideration when crocodilian meat is destined for human consumption (see also p. 130).

Diseases of the Endocrine System


Thymic necrosis In the thymus of crocodiles, small lymphocyte-free groups of medullary stromal cells are frequently observed, some of which are in the process of necrosis. These are believed to be the equivalent of Hassals corpuscles of mammals. Granulomas surrounding a central mass of necrotic heterophils and consisting, in acute cases, of large macrophages, in chronic cases mainly of multinucleated giant cells (Fig. 7.35), were found in the thymus of

Muscle parasites A Trichinella sp. was found in the meat of crocodiles from several farms in Zimbabwe (Foggin and Widdowson, 1996; Foggin et al., 1997; Mukaratirwa and Foggin, 1999) (see p. 197) and third-stage larvae of Gnathostoma procyonis in the meat of American alligators

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Fig. 7.35. Thymic necrosis: necrotic focus surrounded by multinucleated giant cells in a juvenile farmed Nile crocodile.

a large number of slaughtered crocodiles from four different farms (Penrith and Huchzermeyer, 1993), as well as in routine post-mortem material (authors cases). These granulomas appeared to be associated with the above-mentioned non-inammatory lesions thought to be equivalents of Hassals corpuscles. They differ morphologically from the thymic cysts of other reptiles, which characteristically are lined by an epithelium (Bockman, 1970). The possible causes of the inammation could not be established and the question remains whether these granulomas are a pathological phenomenon or part of the physiological processes in the thymus of crocodiles. Foci of colliquation necrosis surrounded by multinucleated giant cells have also been observed in farmed Nile crocodiles (Fig. 7.36) (authors own material). A thymic cyst (Fig. 7.37) found in a routine post-mortem case in a juvenile farmed Nile crocodile was thought to have been a congenital malformation (authors own material).

(see p. 21). The normal histological structure of the parathyroid glands consists of parenchymal cellular cords associated with strands of connective tissue and blood capillaries (Clark, 1970; Oguro and Sasayama, 1976). In cases of nutritional bone disease, in particular osteomalacia and osteoporosis (see p. 211), a transformation and degeneration of the parenchyma is seen, often with the formation of cysts (Fig. 7.39) (authors cases). Parenchymal degeneration and cyst formation were also found in a parathyroid of a severely stressed wild-caught African dwarf crocodile (p. 130) (authors case). This observation raises the question as to whether severe stress can affect parathyroid function, and thus also play a role in the aetiology of bone disease.

Thyroid pathology Occasionally inammation, degenerative changes and cysts were found in crocodile thyroids during routine post-mortem and histopathological examinations of juvenile farmed crocodiles (Figs 7.407.44) (authors cases). These changes did not appear to be associated with any particular clinical manifestation, nor could their causes be estab-

Parathyroidosis The parathyroid gland is surrounded by lobes of the thymus and embedded in fat tissue and therefore difcult to nd (Fig. 7.38)

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Fig. 7.36. Focus of colliquation necrosis surrounded by multinucleated giant cells, juvenile farmed Nile crocodile.

Fig. 7.37. Thymic cyst in a juvenile farmed Nile crocodile.

lished, except possibly for a case of C-cell hyperplasia in the thyroid of a severely stressed wild-caught African dwarf crocodile, which might have been due to prolonged severe stress (see p. 130) (authors case). Cases of goitre have been found in snakes, also without determined causes (Topper et al., 1994).

Stress Stress is one of the defensive functions of the body and is regulated by the central nervous

and endocrine systems. The defensive reaction is in direct proportion to the intensity of the insult, the stressor. As the two, the stressor and the response, are practically inseparable, they are commonly both referred to as stress. The defensive reactions may exert negative inuences on certain other systems. Failure to cope, particularly in captive and farming situations, where crocodiles may be subjected to excessive, continuous or repetitive levels of stress, may lead to a breakdown, with consequent disease and mortality. In this sense

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Fig. 7.38. Cystic Nile crocodile parathyroid gland surrounded by lobes of the thymus.

Fig. 7.39. Cystic degeneration of the parathyroid gland of a juvenile farmed Nile crocodile suffering from nutritional bone disease.

stress can also be regarded as a disease condition of the endocrine systems involved in it, particularly the adrenal glands. The consequences of stress reactions and their implications for the course of certain diseases, but also on the management of captive and farmed crocodiles, are discussed in the following section. They also play a major role in all of the multifactorial diseases (see p. 226). Foci of necrosis were found in the adrenals of a wild-caught African dwarf crocodile

which had been subjected to severe and prolonged stress (see p. 130) (authors material).

Miscellaneous Pathological Conditions


Some of the conditions dealt with in this section are quite unimportant, but were included for the sake of completeness. Others are important but have been inserted here as they did not seem to t into any of

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Fig. 7.40. Thyroiditis in a farmed Nile crocodile.

Fig. 7.41. Goitre in a farmed Nile crocodile.

the preceding sections. While some logic was involved in deciding names, sequence and contents of sections, there also was a certain amount of arbitrariness.

Stress Physiology The physiology of stress in crocodiles has been researched extensively (Lance and

Lauren, 1984; De Roos et al., 1989; Elsey et al., 1990a,b, 1991; Mahmoud et al., 1996; Morici et al., 1997; Turton et al., 1997; Lance and Elsey, 1999a,b). To a large extent the reactions are similar to those in other reptile, avian and mammalian species, with an increased production of adrenaline and corticosteroids. Stressors Some of the stressors important for crocodiles have been identied. They are:

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Fig. 7.42. C-cell hyperplasia in the thyroid of a severely stressed wild-caught African dwarf crocodile.

Fig. 7.43. Large cyst on the right thyroid of a farmed Nile crocodile.

Capture and restraint (Elsey et al., 1991; Mahmoud et al., 1996; Lance and Elsey, 1999b). This includes handling, taking blood samples, giving injections, forcefeeding and other such actions, all placing the crocodile in a situation from which it cannot escape. It appears, though, that

young hatchlings are more tolerant of handling, provided it is done gently. This may have to do with the observation that crocodile mothers will occasionally carry their hatchlings in their mouths. Transport (Elad et al., 1987). While this is also part of restraint, it may further entail

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Fig. 7.44. Section of a cystic thyroid of a farmed Nile crocodile.

disorientation in the new location, with the necessity to establish a new territory, as well as possibly having to cope with a sudden climatic change. All this is part of an inability of the crocodile to move freely and choose its own territory. Cold and sudden change in temperature (Turton et al., 1997; Lance and Elsey, 1999a). The major factor here is an inability to thermoregulate. Captive and farming conditions often restrict or limit the thermogradient available to the crocodiles and which is necessary for an active thermoregulatory behaviour. Overheating (Turton et al., 1997). Here also there is an inability to escape the heat and to thermoregulate actively following an environmental thermogradient, nonexistent in this case. High stocking density (Elsey et al., 1990a,b; Morpurgo et al., 1992). Overstocking causes an inability to move away from other individuals. While hatchlings in the wild live in shoals for some time, juveniles tend to move around, away from adult crocodiles, but also away from other juveniles. The degree of territorial tolerance is different in different species, but in general the same principle applies to all crocodilian species. Adult breeding crocodiles of some species may need fairly large indi-

vidual territories, particularly species that live in pairs. However, it appears that adult farm-reared crocodiles are less territorial than wild-caught breeding stock of the same species. Fear (Watson, 1990). This is an inability to get away from frightening experiences or expected events. Capture and handling of some of the crocodiles on a farm causes the other crocodiles in the same pen to fear that the same might happen to them, and from this they cannot escape. Hatchlings are afraid of birds ying overhead. To escape them, they want to go under cover. Even inside a rearing house, the ceiling or roof above is not perceived by them as cover. Such a cover must be close to the ground. Consequently fear is caused by certain events, but the stressful part is the inability to escape or take cover. The inability to do what is instinctively demanded in any of the above situations can also be translated as frustration, and this leads to the simple equation: frustration = stress. It follows that stress, at least initially, is a psychological problem. Several events causing frustration can happen concurrently and thereby have an additive effect. This effect does not only depend on the severity of the stress or stresses, but also on their duration.

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Effects Short-term stress, with its adrenaline surge, can have a stimulating effect, but of importance are the nefarious effects of longer or severe exposure to stress. Not all the effects below have been conrmed experimentally in crocodiles. However, they occur widely in all higher vertebrates and most of them have at least been observed in crocodiles in real situations. Immune suppression is caused by increased levels of corticosteroids in the circulation. It does not only affect specic immunity, but also the short-term, nonspecic immunity, which in domestic fowls occurs between 6 and 72 h after stimulation with an antigen (Matsumoto and Huang, 2000). Immune suppression by stress can be compounded by the suppression of the immune system at low body temperatures. Consequently, exposure to stress (capture, transport) during winter can have more serious consequences than during summer. Blood corticosteroid levels and white blood cell counts depend on a number of extraneous factors (Turton et al., 1997). While their determination in experimental work is valuable, there appears to be a limit to their usefulness as clinical tools. Disturbance of the mucosal barrier of the intestine. Normally, intestinal bacteria are transported across the mucosal barrier for presentation to the immune system and the production of specic antibodies. Several mechanisms have been studied in mammals (Fields et al., 1986; Neutra et al., 1996; Neutra, 1998; Nadler and Ford, 2000) and they are believed to apply to crocodiles as well. Gut translocation is known to occur in human patients suffering from trauma and shock, resulting in septicaemia (Deitch et al., 1996). Cases of septicaemia involving intestinal bacteria have been seen in crocodiles suffering from severe stress (Huchzermeyer, 2000). This phenomenon has been given the name stress septicaemia (see also p. 228) and it appears to play a major role in the pathology of captive and farmed crocodiles. Fungi can also be translocated across the

mucosal barrier and cause fungaemia. Many of the intestinal fungi of crocodiles are cryophilic and will thrive at low temperatures, at which bacteria may not be able to multiply (see p. 182). Captive American alligators that had been translocated to a hibernation grotto and accidentally subjected to very cold temperatures developed generalized fungal infections (Fromtling et al., 1979a,b). Fungal infection of the lungs does not need the inhalation of fungal spores, but can also take place via the blood circulation, proven at least in ostriches (Walker, 1912). Substance depletion. Certain substances necessary for the metabolism of the host become depleted under stress. Studies in the domestic fowl have demonstrated stress-induced vitamin C depletion in the adrenal glands (Perek and Eckstein, 1959). The lowering of plasma zinc levels under stress conditions in domestic species has been reviewed by Hambridge et al. (1986). No such work has yet been carried out in crocodiles. In some cases it may be possible to counteract the deleterious consequences of stress by supplementing the depleted substances. See Note Added at Proof, p. 239. Disturbed behaviour. In ostriches the disturbance of normal behaviour patterns is a major consequence of exposure to stress (Huchzermeyer, 1998a). To some extent this appears to happen in stressed crocodiles as well. Three disturbed behaviours can be identied: anorexia, hydrophobia and excessive lithophagy (p. 289). Anorexia may be complete or involve the refusal to eat less palatable feeds (p. 282). It is a major cause of runting (p. 234). Hydrophobia is the refusal of stressed crocodiles to go into the water. It is one of the causes of dehydration (p. 283) and gout (p. 230). While lithophagy is seen as part of the normal behaviour spectrum of crocodiles, excessive lithophagy, involving stones as well as many other foreign objects, must be seen as pathological and may necessitate surgical intervention (pp. 36, 94 and 254). The disturbed behaviour of crocodiles can be used to diagnose stress.

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Treatment The most important aspect of the treatment of stress-related conditions is the recognition and removal of the stressor. This cannot be done in the laboratory. The consulting veterinarian may have to visit the farm to investigate present and past conditions and occurrences that could have precipitated the problem. The time scale of stress-related processes depends on the size of the crocodile, as well as on environmental temperatures. Juvenile crocodiles in a heated house may show signs of stress septicaemia within 10 days, while adult crocodiles translocated during winter may die several months after the event. Depleted substances can be supplemented. The benecial effect of supplementation with vitamin C to stressed poultry has been documented (Gross, 1992) as well as its effects on the immune system (Bendich, 1990). It prevents the slide in heterophil/ lymphocyte ratios and also increases resistance against infection. Some adrenal-blocking agents may well warrant further investigation and experimentation in crocodiles. Substances that have been tried in poultry are ketoconazole (Pont et al., 1982), as well as dichlorophenyldichloroethane (Rothane, ICN Pharmaceuticals) and Metyrapone (Ciba Geigy) (Gross, 1990). However, in most cases such chemotherapy will come too late, if mortality from stress-related conditions has occurred already. Fungal and bacterial infections precipitated by stress may warrant specic treatment, depending on the agent. For the treatment of anorexia see below.

be avoided, there may be several courses of action, such as tranquillization/immobilization (see p. 70), which not only reduces the level of stress in the animal to be captured and handled, but also in the other crocodiles witnessing the event. When environmental stressors are involved, prophylactic supplementation with ascorbic acid (vitamin C) should be considered.

Anorexia While it has been reported that anorexia in hatchlings may be caused by an unsuitable diet, e.g. minced sh (Foggin, 1992a), all evidence points at stress as the main cause (see above), with stressed animals being less likely to accept an unpalatable diet, such as minced sh or pelleted feed (see also p. 289). Hatchlings most commonly become stressed by fear and uctuating temperatures, including occasional overheating. In older crocodiles anorexia is often triggered by handling and transport. Once a crocodile has stopped feeding, it becomes hypoglycaemic, and the hypoglycaemia further suppresses the appetite. Such animals may simply starve to death, if they are not killed earlier by a concomitant stress septicaemia (see p. 228). The only way to break this slide towards death is by stimulating the appetite in one way or another, while at the same time optimizing environmental conditions. This must be done without drastic changes that could further stress the animal. One can try moving food in front of the animals head, enticing it to snap, or, for hatchlings, some insects (cockroaches or crickets) can be released into their pen. On one Nile crocodile farm with semi-open rearing pens, a light was suspended high above each rearing pen and the hatchlings jumped at the insects which fell down after ying into the light (see Fig. 3.11). If these attempts fail in larger crocodiles, one can tap the crocodile on the snout with a stick. The crocodile then will open its mouth and one can place a morsel of food, possibly injected with a multivitamin preparation, into its mouth and wait for the morsel to be

Prevention The prevention of stress must primarily be based on the prevention of stressful conditions and occurrences. These have been discussed above in detail, and this knowledge should be applied to all captive and farming installations and their management. All handling of crocodiles should be done with minimum fuss, quietly and as gently as possible. Where stressful situations or events cannot

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swallowed. If the morsel is rejected and the mouth is opened after another tap on the nose, an amount of thick sugar solution or honey is smeared on to the base of the tongue. Most of this sugar or honey will be swallowed slowly and absorbed. It will cause the blood sugar level to rise, and after possibly two or three such applications, one each day, normal feeding may resume. Alternatively, subcutaneous injections (see p. 89) of a glucose solution, and possibly also multivitamins, can be given. Small hatchlings tolerate handling more easily and can be force-fed (see p. 87) a sugar or glucose solution, or a more complex nutrient uid, e.g. one cup of milk with one hens egg yolk and a tablespoon of sugar or glucose. Stimulation of the appetite by oral dosing with metronidazole (Flagyl) 125250 mg kg 1 has also been suggested (Thurman, 1990). Gastric function in ostrich chicks suffering from gastric stasis, also a stress-related condition, is restimulated by the injection of metaclopramide 0.1 mg kg 1 live mass (Huchzermeyer, 1998a). The loss of salt into the water (p. 41) can be counteracted by adding salt to the water 1 g l 1 (p. 86) or by dosing with a liquid containing salt, e.g. meat broth (Sinha et al., 1987) (see p. 253).

should be combined with the treatment for that condition (see above). The same considerations also apply to optimizing environmental conditions. In addition, physiological saline solution can be given by injection, and hatchlings can be dosed with uids by mouth (see p. 86).

Neoplasms Not all swellings found on or in crocodiles are true neoplasms. Pseudotumours are caused by the inammatory process now called briscess, which takes place around localized bacterial infections, particularly septic wounds (Huchzermeyer and Cooper, 2000) (see also pp. 46 and 287). All of the growths recorded in C. johnsoni (Webb and Manolis, 1983) apparently fall into this category. Granulomata are caused by localized fungal infections, commonly seen externally in skin abrasions and internally in cases of stress-associated generalized mycoses (see pp. 182 and 281). The surgical removal of such a granuloma from the palatal fold of the basihyal valve of a captive C. palustris and the removal of digital granulomata from a captive American alligator have been reported (Ensley et al., 1979; Russo, 1979). Smaller digital granulomata could have been misdiagnosed as warts, which were reported during a discussion at a meeting without any further details (Schlumberger and Luck, 1948). A wart-like structure on the dorsum nasi was found in a captive male American alligator (Wadsworth and Hill, 1956). The wart-like appearance of such granulomas is shown in Fig. 7.45. True warts, papillomas, have not been described from crocodiles and there are only very few reports of other neoplasms in crocodiles: A captive male American alligator died from a very large seminoma attached to the dorsal wall of the abdominal cavity (Wadsworth and Hill, 1956). A round cell tumour was found in the liver with metastases in the cerebellum and heart in a captive C. porosus (Scott

Dehydration While dehydration can occur during a long period of transport, rehydration will occur when the transported animals are released into the water. However, care must be taken that they have fully recovered from chemical immobilization (see p. 70) before they are given access to water, because otherwise they might drown (see also p. 290). Refusal to go into the water, hydrophobia, is one of the manifestations of stress and should be seen as a behavioural disturbance (see pp. 278 and 289). It is the most common cause of dehydration. Severe dehydration can cause a malfunctioning of the kidney, leading to gout (see pp. 230 and 264). As stress-induced dehydration is always associated with anorexia, its treatment

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Fig. 7.45. Wart-like appearance of fungal granulomas on the toes of a juvenile farmed Nile crocodile.

and Beattie, 1927). Later this tumour was re-interpreted as lymphosarcoma (Schlumberger and Luck, 1948). A polycystic ovarian mesothelioma was found in an adult captive Crocodylus acutus (Obaldia et al., 1990). A brosarcoma was found to obstruct the oropharynx of a captive adult male Crocodylus siamensis (Janert, 1998). A chondroma was excised from a juvenile captive Caiman latirostris (personal communication, J.C. Troiano, Buenos Aires, 1999). A stalked mass attached to the left hind foot of an adult crocodile was diagnosed as broma and a bulging mass on the back of the thorax of an adult crocodile as lipoma (Youngprapakorn et al., 1994). Bone tumours of undetermined nature were found on museum skeletons of two Caiman crocodilus (Klin, 1936).

Injuries Crocodiles are prone to injuries through intraspecies aggression in the wild as well as in captive and farming systems. In juvenile farmed Nile crocodiles, aggression was related to body size, stocking density and food preference, and directed mainly by larger towards smaller individuals (Morpurgo et al., 1993b). Sexually mature crocodiles may ght for territory, the possession of a female or over a nesting site. In captive and farming situations, where there is no escape for the loser, hierarchical ghts may take place again and again (see p. 54). Injuries sustained may be series of skin punctures, raking wounds across an area of the skin, deep gashes, amputations of toes, of part of the tail and even whole limbs. Part of the upper or lower jaw may be broken or severed (Figs 7.477.49) and deep penetrating bite wounds may injure the internal organs, leading to further complications, such as intestinal occlusion (see p. 258) or peritonitis (Schoeb, 1999). Most likely this latter case had resulted from a bite wound as well. Interspecies interactions are far less important and, with the exception of other crocodile species, mainly involve hunting injuries caused by man, such as a native spear imbedded in the back of a Nile croco-

Cysts were found on the skin of hatchling crocodiles, as well as in the mesentery and in the salivary glands of adult crocodiles (Youngprapakorn et al., 1994), also under the eye (Plate 24) and near the nostrils (Fig. 7.46). They are probably due to blockages of glandular ducts. See also gonad cysts (p. 266), thymic cyst (p. 274) and thyroid cyst (p. 275).

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Fig. 7.46. Cyst near the nostrils of a captive Nile crocodile (photo Marc Gansuana).

Fig. 7.47. Nile crocodile hatchling with amputated upper jaw and broken lower jaw.

dile and penetrating its stomach (Hippel, 1946), but also gunshot wounds and injuries caused by rough handling during capture. All injuries occur in a septic environment and penetrate the skin, which often is colonized by intestinal bacteria. Consequently, all these injuries can be regarded as septic. However, cases of septicaemia contracted

from such wounds are extremely rare. This is due to the immobilization of the bacteria in the wound by the exudation of brin (briscess formation, see pp. 46 and 287), which prevents the draining of infected lymph into the general circulation. Healing usually is rapid, but briscesses in deep wounds, or damage to internal

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Fig. 7.48. Adult farmed Nile crocodile with amputated upper jaw.

Fig. 7.49. Captive gharial with amputated upper jaw.

organs, may have more serious consequences. However, regeneration is limited and recorded only for parts of the upper jaw (Brazaitis, 1981) and the tip of the tail (Klin, 1936). The regenerated tail tip may be covered by a uniform layer of keratin. The tail abnormality depicted by Troiano and Romn

(1996) also appears to be a regenerated tail tip. Where the treatment of a wound necessitates the capture and immobilization of the animal, one must consider the stress caused by such an action and weigh the danger of a localized wound infection against the possi-

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bility of causing stress and septicaemia (see pp. 228 and 278) by the necessary use of force. Where the wound is accessible, it should be cleaned out with a cotton swab and a 10% solution of hydrogen peroxide, and all necrotic tissue and brin should be removed. The cleaned wound should be treated liberally with a proteolytic enzyme spray, left for a few minutes and than sprayed with a gentian violet spray (Flamand et al., 1992). If at all, only absolutely clean wounds should be sutured, and local anaesthesia should be used for this procedure (see p. 92).

Abscesses Infected local swellings have, in the past, been referred to as abscesses. However, they do not contain pus but brin, and in crocodiles they are not encapsulated, nor are they associated with necrotic processes (Fig. 7.50). The term briscess has been proposed to differentiate this type of swelling or pseudotumour from true abscesses (Huchzermeyer, 1999; Huchzermeyer and Cooper, 2000) (see also p. 46). A persistent infection may cause the continuation of brin exudation and thereby a slowly increasing growth of a briscess.

Where such a swelling does not interfere with the normal functions of the body, it is best to leave it alone. However, if a surgical intervention does become necessary, care must be taken to remove all traces of brin, disinfect well, use a proteolytic enzyme spray and also an antibacterial powder or spray before closing the wound. Handling and immobilizing the crocodile, as well as transferring it to a clinic for the operation, may already cause stress (see p. 278). Keeping the treated crocodile out of the water to prevent re-infection of the wound may cause further stress, as well as dehydration (see p. 283). These points should be taken into account when a surgical intervention is considered.

Arthritis Arthritis limited to one joint can be caused by a septic injury penetrating the joint (see also p. 284). However, much more common in crocodiles is polyarthritis, the inammation of many joints at the same time, which is a common sequel to non-specic septicaemias (see pp. 173 and 228). The only specic disease associated with polyarthritis is mycoplasmosis (see p. 167).

Fig. 7.50. Juvenile farmed Nile crocodile with briscess formation under the sternum as the consequence of a penetrating bite wound.

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Usually the area around the joint becomes swollen and the animal is unwilling to use the affected legs. Note that in poikilothermic animals the temperature of the affected joint is not elevated. An inability to move can also be caused by nervous disorders, such as encephalitis (see p. 266) and meningitis (see p. 267), by the fracture of a vertebra (see p. 267) or by white muscle disease (see pp. 219 and 274). On post-mortem examination of cases of arthritis, one nds either increased quantities of synovial uid, clear yellowish or turbid in early cases, or dry deposits of brin. Bacterial culture will reveal the presence of the causative organism. There is no treatment. Note that some of the anti-inammatory drugs, which one might be tempted to use, are nephrotoxic (see p. 226). The prevention of arthritis is based on the prevention of stress, as stress is the one factor that triggers septicaemia (see p. 278). Interdigital emphysema: bubble foot Gas bubbles forming in the interdigital skin folds (web) on the feet of crocodile hatchlings have been seen in C. porosus hatchlings on two farms in Australia (Turton et al., 1996)

and in C. niloticus hatchlings on one farm in Zimbabwe (Fig. 7.51) (authors case). In the Australian case, the bubbles appeared to form in lymphatic spaces and elicited a mild inammatory response. Various bacteria were isolated from the lesions and poxvirus was found on the skin surface, but a causative agent could not be determined. The Zimbabwean farm used water from a hot spring and it is surmised that the water contained gas under pressure which, when drunk by the hatchlings, caused gas to bubble out in the feet, in a fashion similar to gas bubble disease in shes (Wedemeyer et al., 1976). This could be prevented by storing the water in an insulated tank and allowing the gas pressure to equalize, before using the water in the rearing pens.

Frostbite When juvenile American alligators were placed in bags into a freezer to achieve a body temperature of 2.58C in preparation for heart surgery, the extremities of some the alligators were outside the bag and exposed to the extreme cold. In one case this led to frostbite, with the stratum corneum slough-

Fig. 7.51. Interdigital emphysema, bubble foot, in a farmed Nile crocodile hatchling.

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ing off where the scales had been frozen (Kennedy and Brockman, 1965). (Note that the cool room and freezer temperatures stated in this paper (40C and 48C respectively) probably were calculated incorrectly when converting F to C.)

Overheating The optimal body temperature of crocodiles of 3133C is very close to the tolerated upper range of 3536C. The upper-range temperatures can cause severe stress (see p. 278), while a body temperature of 37C can be lethal. The smaller the crocodile, the quicker its body reaches the temperature of the environment. Consequently, hatchlings are more sensitive to overheating than larger juvenile or adult crocodiles. On farms with open or semi-open rearing facilities, the danger of overheating exists as soon as air temperatures rise above 36C, even if the hatchlings can escape into the shade. If shallow water is exposed to the sun, its temperature can rise above 36C as well. This then creates an inevitably lethal situation for the hatchlings.

Crocodiles exposed to extreme temperatures cannot sweat to cool down their body. While they are losing some moisture through the skin, this is not used as a thermoregulatory mechanism to any extent. They have to use the thermogradient in their environment to maintain their preferred body temperature (see p. 55). In many captive and farming systems the range of possibilities for active thermoregulatory behaviour is inadequate (Fig. 7.52). The consequence of overheating stress in hatchlings is anorexia, and in older juveniles an unwillingness to eat unpalatable food (see p. 282). In all age groups there is an increased sensitivity to specic and non-specic infections (see p. 278). In extreme events, mortality, even mass mortality, may occur. Disturbed behaviour Organic diseases Seemingly disturbed behaviour may be caused by central nervous pathology, as in star gazing thiamin deciency (see pp. 217 and 268), and circular movements or loss of

Fig. 7.52. Nile crocodile hatchlings in a small semi-open pen, potentially unable to escape overheating on a hot day.

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balance in cases of encephalitis (see p. 266) or meningitis (see p. 267), by pain as in cases of arthritis (see p. 287) and arthritic gout (see p. 230), as well as by muscular disorders such as myositis and white muscle disease (see p. 274) and also by osteomalacia (see p. 211). Stress True behavioural disturbances are caused by stress (see p. 278). Three forms of behaviour are seen in this category: anorexia or the refusal to accept all or certain foods (see also p. 282); hydrophobia, the refusal to go into water with consequent dehydration (see also p. 283); and excessive lithophagy (see pp. 36, 94 and 278). Fear piling A frightened crocodile will try to seek refuge either in deep water or under shelter. The younger the crocodile, the more serious is its need to escape perceived danger. Piling in a corner of the pen is a normal reaction to fear, sudden fright, but it is aggravated by shallow water, which is not seen as a sufciently safe refuge, and the lack of hide boards, under which the animals would normally seek shelter. Piling is worse under high stocking densities. In this sense piling is not a behavioural problem of the crocodiles but rather a design problem of the rearing facility, a problem of management. While animals used to human presence are less likely to take fright and to pile, the best solution to the problem lies in the provision of hide boards under which the crocodiles will feel safe (see also p. 114). Piling may cause death by suffocation and it can also cause severe damage to the belly skins by scratches caused by the protruding long canine teeth (see p. 241). Good management The stressed-induced behaviour problems discussed above, anorexia, hydrophobia, excessive lithophagy and piling, should not only be seen as problems by themselves but also as indicators of stress on the farm, and their absence as a sign of good management.

Drowning Drowning is diagnosed either when the dead crocodile is found in the water, oating or lying on the bottom, or when on postmortem examination the lungs are found to be lled with water. There are several possible circumstances under which crocodiles may drown, particularly in captive or farming conditions. Mechanical The pen design may be such that hatchlings can get trapped under a heating pipe and drown (see Fig. 7.52), or under any other underwater structure. Tetany Crocodiles suffering from seizures due to hypocalcaemia (see pp. 211 and 267) have been known to drown (Foggin, 1992a). Nervous abnormality Crocodiles suffering from brain disease, such as encephalitis (see p. 266) and meningitis (see p. 267), may not be able to control their movements sufciently to come to the surface for breathing, and consequently may drown. Drugged While recovering from the effects of immobilization (see p. 70), crocodiles may go into the water, before being able to swim to the surface for breathing, and consequently drown. It is important, therefore, that they are denied access to water, even if in danger of dehydration, until they have recovered fully. Weakness Weakness may prevent crocodiles from climbing out of the water area in their pen on to land. If this weakness is caused by osteomalacia (see p. 211), an affected hatchling may be able to swim around for a long time. If the pen design allows, the animal

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may remain on the shallow slope with its head out of the water. However, general weakness of a sick animal may in the end cause it to drown. Agonal Any sudden death may cause a last agonal breath to be taken. If sudden death occurs in the water, such a movement will cause the

lungs to ll with water. In this case the postmortem appearance will be that of drowning, and the true cause of death may remain hidden. Deformities Tailless crocodiles are unable to swim and drown in deep water when they are unable to swim to the surface (see also p. 149).

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Index

Abattoir 123124 Abdominal wall defects 155 Abrasions see Skin Abscess see Fibriscess Acanthocephala see Hookworm Acanthostomum atae 200 caballeroi 200 coronarium 200 diploporum 200 elongatum 200 loossi 200, 203 marajoarum 200 pavidum 200 productum 200 quaesitum 200 scyphocephalum 201 vicinum 201 Acidbase balance 41, 43, 47 Acinetobacter 37 anitratus 38 calcoaceticus 38 wolf 38, 130 Acremonium sp. 40 ACTH 91 Adenovirus 74, 117, 157, 160161, 167, 228, 234, 256, 259, 271272 Adrenal 22, 79, 218, 277 blocking agents 282 necrosis 277 Adrenaline 43, 91, 278 Advocin see Danooxacin Aerobacter radiobacter 38 Aeromonas 37 hydrophila 38, 39, 67, 142, 173, 225, 239 shigelloides 173

Aestivation 41, 44, 55 African dwarf crocodile see Osteolaemus tetraspis African slender-snouted crocodile see Crocodylus cataphractus Age 101, 116 determination see Bone rings lengthweight relations 3435 Agema silvaepalustris 207 Aggression see Fighting Albendazole 197 Albinism 154 Albumin 48, 49 Alcaligenes denitricans 130 faecalis 39 Algal toxins 224 Algicides 224, 225, 231 Alkaline tide see Acidbase balance Allechinostomum crocodili 201 Alligator mississippiensis 4, 7, 18, 22, 24, 25, 28, 30, 34, 35, 3738, 40, 42, 43, 44, 4546, 47, 48, 49, 50, 51, 52, 56, 67, 68, 70, 71, 91, 92, 93, 94, 95, 96, 99, 100, 101, 102, 113, 117, 121, 123, 125, 129, 139, 141, 146148, 149, 151, 154, 155, 163, 167, 172, 173, 174, 176, 177, 178, 183, 190, 192, 193, 197, 199, 200, 201, 202, 203, 204, 207, 208, 219, 221, 222, 223, 224, 230, 231, 239, 240, 244, 245, 246, 247, 254, 259, 262, 265, 266, 267, 269, 270, 271, 272, 274, 281, 283, 288 sinensis 4, 9, 28, 52, 56, 170 Alligator hatchling syndrome 146148, 172 Allometry 34 323

324

Index

Aloa ginae 207 indica 207 merki 207 nilotici 207 parva 207 platycephala 207, 208 simpsoni 207 Alphaxolone/alphadolone 94 Aluminium 222, 223 Amblyomma dissimile 205 grossum 205 sp. 205 American alligator see Alligator mississippiensis American crocodile see Crocodylus rhombifer Ammonia 41, 48, 49, 50, 111, 121, 135, 230 Amoebae 192 , 258 Amprolium 90, 188 Anabolic steroids 102 Anaemia 221, 269 Anaesthesia 92, 93, 95, 138, 287 Anasarca 217 Anastomosis 23 Anectine see Succinylcholine Angiotensin 43 Anopheles stephensi 198, 205 Anophthalmia 152, 153 Anorexia 148, 160, 164, 167, 181, 182, 221, 226, 234, 237, 250, 251, 253, 262, 281, 282, 289, 290 Antibiotics 91, 101, 146, 161, 166, 217, 225, 241, 273 residues 102, 130 resistance 89, 91, 102, 146, 225 Anti-inammatories 226, 231, 288 Antioxidant 100 Ants see Solenopsis Aponomma exornatum 205 Appetite 112, 136 suppression 138, 282 seasonal 37, 113, 230 Archaeodiplostomum acetabulatum 201 Arsenic 222 Arteritis 237, 252, 269, 270 Arthrinium sp. 40 Arthritis 79, 174, 229, 231, 252, 273, 287288, 290 Articial insemination 123 Ascaridoids 192194, 229, 252 Ascites 148, 167, 221, 234 Ascorbic acid see Vitamins, C Aspergillus 141, 177 clavatus 40 avus 40, 176 avipes 38 fumigatus 176, 178 niger 40, 141, 176

ustus 176, 178 versicolor 176 Atresia bile duct 155 intestine 155 Atrophocaecum acuti 201 americanum 201 caballeroi 201 Axial deformities 149151

Bacillus alvei 39 cereus 39 circulans 39 coagulans 39 lentus 130 sp. 37, 38, 174 Bacterial resistance see Antibiotics, resistance Bacterial translocation 228229 Bacteriology sampling 82, 84, 86 Bacteroides asaccharolyticus 37 bivius 37 denticola 37 loeschei 37 oralis 37 sordellii 37 thetaiotamicron 37 vulgatus 37 Banding see Egg Barbiturates 92, 93 Basking 44 Basophils 25 Baycox see Toltrazuril Baytril see Enrooxacin Beauveria 40 bassiana 176, 178, 182 Behaviour 5256, 245 disturbed 95, 230, 254, 281, 283, 289290 requirements 137 Beryllium 222 Bilirubin 48 Bile 161 stula 96 medicinal use 132 Biochemistry 4752 blood 4749 fat 4951 minerals 4950 skin glands 52 urine 4849 Biodiversity 182, 192 Biopsy 67 Biosecurity 117118 Biotin deciency 100, 221, 237

Index

325

Black caiman see Melanosuchus niger Blastocystis sp. 192 Blepharo-conjunctivitis see Conjunctivitis Blindness 149, 169, 245, 247 Bloating 252 Blood biochemistry see Biochemistry blood cells 24 circulation 43 enzymes 48, 49 lm 6465, 82, 84 ow 43, 44 parasites 188, 190, 191, 202, 203, 268269 pressure 43 sampling 24, 6465, 82, 84 shunt 43 volume 24 Bollinger bodies 158, 159 Bone minerals 49 rings 34, 85 tumours 284 Bornean crocodile see Crocodylus raninus Borrel bodies 158, 159 Botulism 224225 Brachycephaly 152 Bradycardia 43 Brain 27, 44, 80, 124, 133, 223, 283, 290 malformations 153 parasites 268 petechiae 267 Breeding 118123, 136 Brevidi E see Suxathonium Brevimulticaecum baylisi 192 gibsoni 192 pintoi 192 stekhoveni 192 tenuicolle 192 Broad-snouted caiman see Caiman latirostris Bronchopneumonia 271 Brown spot 172, 240 Burrowing 44, 5556 Bush meat 130

Cadmium 222, 223 Caenorhabditis sp. 198 Caesium 224 Caiman crocodilus 4, 18, 19, 22, 25, 28, 37, 39, 52, 68, 71, 93, 94, 96, 99, 101, 102, 129, 141, 152, 154, 158, 163, 170, 171, 174, 176, 177, 182, 183, 184, 190, 192, 193, 196, 197, 198, 199, 200, 201, 202, 203, 205, 207, 208, 219, 221, 224, 226, 231, 246, 252, 266, 267, 270, 284

latirostris 4, 25, 28, 48, 49, 52, 68, 123, 167, 183, 190, 192, 201, 203, 207, 284 Caimanicola marajoira 201 Calcium 100, 103, 136, 139, 148, 211, 213, 230, 249, 265 deciency 6263, 102, 148, 267, 272 EDTA 223 plasma 42, 48, 49, 50, 266 urine 50 Calcium-borogluconate 90, 213, 253 Calls see Vocalization Campylobacter fetus 38, 174 Candida 38, 176 albicans 176, 181 guillermondii 40 humicola 38 krusei 40 lipolytica 38 parasilosis 176 rugosa 38 zeylansides 38 Cannibalism 37, 5354, 74 Cap-Chur Barb see Pentobarbital Capillarioids 194196 Capsulodiplostomum crocodilinum 201 Captive bolt gun 76, 124, 125, 138 Capture 5760, 137, 138, 229, 245, 279, 285, 286 Carbohydrate 101 Carcass yield 128 Cardiac hypertrophy 269 Cataract 247 Cephalosporium sp. 176, 178, 182, 274 Cestode 192, 203, 256 larvae 130, 203, 274 Chinese alligator see Alligator sinensis Chlamydia 74, 117, 130, 157, 167170, 246, 247, 260, 262 psittaci 167 Chlamydiosis see Chlamydia Chloramphenicol 90, 247 Chloride 48, 49, 50 Cholecystitis 262, 272 Cholecystotomy 96 Choleliths 262 Cholesterol 48, 49, 50, 51, 129 Choline 99 Chondroma 284 Chorioretinitis 247 Chromium 99, 222, 223 Chromobacterium sp. 174 Chromosomes 27, 33 Chronic stress dermatitis 173, 237239, 240, 241, 245, 250, 252, 270 Chrysosporium sp. 40 Circulation see Blood Citrobacter 37, 38, 39, 141, 174 amalonaticus 38, 39 freundii 38, 39, 174

326

Index

Cladosporium sp. 38, 176 Claw abnormalities 273 Clitoral appendage see Clitoris Clitoris 19, 70 Clitoropenis see Clitoris Cloaca 17, 62, 70, 79, 128, 140, 200, 263, 265 examination 70 glands see Skin glands ulceration 221, 259 Cloacitis 259 Clostridiosis 172 Clostridium 37, 172 bifermentans 37 botulinum 224 clostridioforme 37 limosum 37, 172 perfringens 259 septicum 172 sordellii 37 tetani 37 CO2 excretion 41 Cobalt 99, 223 Coccidia 53, 74, 117, 141, 157, 182, 228 Coccidiosis 183188, 234, 256, 262, 271 Colibacillosis 190 Coliform bacteria 142 Colitis 257258 Common caiman see Caiman crocodilus Competitive exclusion 38, 145, 227 Conjunctivitis 62, 87, 163, 245247, 266, 270 chlamydial 87, 167170, 217 Contracaecum sp. 198 Copper 50, 99, 100, 222, 223 sulphate 173, 177 Coracoid 7, 77 Corneal perforation 247 Coronavirus 163, 257 Corpora lutea 18 Cortisone 49, 91 Corticosteroids 117, 126, 218, 278, 281 Corynebacterium 38, 174 pyogenes 174 Creatinine 48, 49, 50 Crocodilicola caimanicola 201 gavialis 201 pseudostoma 201 Crocodilocapillaria longiovata 194 Crocodylus 1 acutus 1, 28, 41, 72, 95, 171, 183, 193, 195, 196, 200, 207, 223, 240, 247, 273, 284 cataphractus 1, 28, 190, 192, 193, 201, 202, 207 intermedius 1, 28, 193, 196, 247, 273 johnsoni 1, 2, 24, 28, 41, 49, 51, 69, 70, 72, 92, 94, 129, 149, 153, 158, 170, 174, 193, 194, 195, 196, 200, 201, 202, 203, 204, 205, 207, 208, 231, 241, 249, 268, 274

mindorensis 1 moreletii 1, 28, 48, 71, 102, 151, 195, 196, 205, 221, 254 niloticus 1, 18, 28, 35, 39, 40, 41, 44, 48, 49, 51, 61, 68, 72, 73, 74, 91, 92, 93, 94, 98, 99, 102, 117, 119, 120, 134, 141, 151, 152, 154, 158, 160, 162, 163, 167, 170, 173, 174, 176, 177, 178, 179, 181, 182, 183, 184, 188, 190, 192, 193, 196, 197, 198, 200, 201, 202, 204, 207, 217, 218, 219, 221, 222, 225, 231, 234, 235, 238, 241, 243, 246, 247, 248, 249, 250, 251, 252, 254, 256, 257, 258, 259, 262, 264, 265, 266, 268, 269, 270, 271, 272, 274, 282, 284, 288 novaeguineae 1, 28, 52, 152, 174, 184, 190, 193, 194, 195, 196, 198, 202, 203, 207, 208, 231, 265, 268 palustris 1, 19, 28, 72, 92, 95, 174, 184, 190, 193, 196, 201, 207, 249, 253, 266, 271, 283 porosus 1, 24, 28, 34, 40, 41, 45, 48, 51, 67, 69, 70, 72, 98, 99, 129, 141, 149, 152, 158, 170, 174, 176, 177, 181, 182, 184, 190, 192, 193, 194, 195, 196, 197, 198, 200, 201, 202, 203, 204, 207, 217, 224, 231, 234, 244, 246, 265, 267, 268, 274, 284, 288 raninus 1 rhombifer 1, 24, 28, 52, 68, 193, 199, 200, 201, 202, 203, 219, 220, 223 siamensis 1, 28, 167, 201, 202, 207, 284 Cross-breeding 43, 134, 136 Cryptococcus lipolytica 40 luteolus 40 Cryptosporidia 188 Cuban crocodile see Crocodylus rhombifer Culex dolosus 205 Curvularia 38, 40, 177 lunata 176 Cuviers dwarf caiman see Palaeosuchus palpebrosus Cyatocotyle brasiliensis 201 crocodili 201 fraternae 201 Cyclopia 153 Cysts 266, 275, 284 Cystodiplostomum hollyi 201

Danooxacin 90 Darting 71 Dectomax see Doramectin Dehydration 95, 230, 233, 234, 235, 251, 264, 281, 283, 287, 290

Index

327

Dental anomalies 152, 247249, 273 mineralization 249, 273 Dermacoccus nishinomyaensis 39 Dermatitis 170, 177, 237239, 240 fungal 177178, 240241 Dermatophilosis see Dermatophilus Dermatophilus sp. 172173, 236, 240, 244 Deuritrema 202 gingae 202, 265 Diarrhoea 164, 228 Diazepam 71, 72 Digenetic trematodes see Trematodes Digestion 3637, 101 Diphtheroides sp. 38 Diplostome 201 Disease 46 Disinfection 105, 107, 113114, 118, 124, 126, 141, 143, 145, 146, 158, 166, 170, 173, 177, 186, 226, 228, 237, 241, 242, 244, 245, 247, 250 Dislocation 137 Dispersal of juveniles 53 Distoma pyxidatum 201 Diving 40 DNA 1, 121 Doramectin 90, 209 Dosing 87 Double scaling 241, 245 Drechsleria sp. 38 Drinking 42 Drowning 70, 71, 111, 212, 290291 Dujardinascaris angusae 193 antipini 193 blairi 193 chabaudi 193 dujardini 193, 194 gedoelsti 193, 194 harrisae 193 helicina 193 longispicula 193 madagascarensis 193 mawsonae 193 paulista 193 petterae 193 philippinensis 193 puylaerti 193 salomonis 193 tasmani 193 taylorae 193 waltonae 193 westonae 193 woodlandi 193 Duodenal loop 16, 79 malformation 155 Duodenum 16, 37, 79

Ear 28, 204 Eastern equine encephalitis virus 163 Echinostoma jacaretinga 201 Ectopia cordis 155 Ectopic eggs 265266 Ectromelia 151 Edwardsiella 37, 174 tarda 38, 174 Egg 3032, 93, 103, 139142, 221, 223 albumen 32, 141 composition 52 banding 31, 101, 103, 121, 139, 140 cleaning 105 collection 60, 103104, 118, 121, 137, 139, 140 examination 86 infertility 86, 140 laying 42, 265 metals 222, 223 shell 31, 103, 141, 223 cracking 106, 139, 141 defects 102, 139, 149 porosity 139 size 33, 34, 42 yolk 31 composition 5152 EKG 64 Eimeria 183, 184 alligatori 183, 184 caimani 183, 184 crocodyli 183, 184 hatcheri 183, 184 kermoganti 183, 184 paraguayensis 183 pintoi 183, 184 Electrocardiogram see EKG Embryo 32, 42, 86, 103, 139, 222 Embryonic death 139, 140 learning 53 Emphysema interdigital 273, 288 lung 178, 262, 272 Encephalitis 163, 246, 256, 266267, 270, 290 Encephalomalacia 267 Endocarditis 269 Endocrine disruption 223244, 266 Endometritis 265 Energy 9899, 101, 129 Enrooxacin 90 Entamoeba sp. see Amoebae Enteritis 82, 87, 145146, 148, 164, 172, 190, 226228, 255258, 266 Enterobacter agglomerans 38, 39, 130, 174 cloacae 38, 39, 141 gergoviae 39

328

Index

Enterococcus 37 caecorum 39 durans 39 faecalis 39 faecium 39 pseudoavium 39 solitarius 39 Eosinophils 25, 67, 204 Epicarditis see Pericarditis Epicoccum sp. 38 Erysipelothrix insidiosa 171, 240 Erythrocytes 24, 189, 190 ESB3 see Sulphachloropyrazine Escaping 109, 111 Escherichia 37 coli 38, 39, 174, 227, 256 hermani 38 Etorphine 71, 73, 94 Eustachian tubes 1112, 77 Eustrongylides sp. 198 Evisceration 124, 128 Excretion see Urine Exophthalmia 153 Exotidendrium 202, 265 gharialii 201 Exudation see Fibrin Eye 28, 62, 76, 173, 245247 defects 153 Eyelids 28, 62, 76, 204, 237, 245, 247

F10 see Disinfection Faeces sampling 66 False gharial see Tomistoma schlegelii False nostrils 13, 153, 249 Fat 99, 100, 101, 113, 129, 131, 146, 178, 222, 225, 228, 230, 243, 245, 250, 259 composition 4951 digestion 37 medicinal use 131 necrosis see Steatitis somatic 29, 245 Fat body 2829, 79, 144, 155, 170, 234 Fat body:heart ratio 86, 245 Fatty acids 4952, 99, 100 Fear 114, 227, 234, 241, 245, 280, 282, 290 Feed efciency 101 selection 53 Feeding 113, 121, 138 Fenbendazole 90, 194 Fever 46 Fibrin 46, 88, 143, 144, 145, 161, 164, 167, 169, 186, 187, 188, 228, 245, 246, 247, 252, 256, 258, 262, 263, 265, 269, 271, 285, 287, 288 Fibriscess 46, 143, 164, 208, 239, 241, 242, 254, 283, 285, 287

Fibroma 284 Fibrosarcoma 284 Fighting 54, 116, 117, 119, 120, 121, 122, 140, 242, 245, 247, 248, 249, 265, 284 Filariae 197 Fire ants see Solenopsis Flagellates 190191 Flavobacterium balustinum 39 breve 130 gleum 38 indologenes 130 indoltheticum 38 multivorum 38 odoratum 39 Flaxedil see Gallamine Flies 109, 111, 118, 188, 191, 205, 228 Flora intestinal 32, 38, 118, 129, 141, 148, 163, 164, 173, 176, 217, 226, 227, 228 oral 37 skin glands 38 Flukes see Trematodes Folic acid 100 Foraging 54 Foramen of Panizza 23, 43 Force feeding 87, 148, 235, 253254, 282283 Foreign bodies, gastric see Stomach Fracture, mandible 95 spinal column 212, 267, 273 Frost bite 288289 Frustration 280 Fungaemia 182, 281 Fungal infection 104, 134, 176182 Fusarium 38, 40, 142, 176, 177, 182 moniliforme 176, 178, 272 oxysporum 141 solani 141, 176, 178, 179, 182 Fusobacterium nucleatum 37 varium 37

Gall bladder 18, 79, 96 Gallamine 71, 72, 73 Gambusia afnis 208 Gamma irradiation 129 Gaping 44, 55 Gastralia see Ribs, abdominal Gastric cannulation 96 Gastric pressure 64 Gastrin 15 Gastritis 87 Gastroenteritis 253254 Gastroliths 15, 36, 95, 254 Gastrotomy 9495, 254

Index

329

Gavialis gangeticus 5, 28, 38, 135, 149, 153, 172, 174, 183, 184, 188, 190, 193, 197, 199, 201, 202, 207, 220, 231, 265 Gedoelstascaris australiensis 193 vandenbrandeni 193 Genetic defects 140, 148, 234, 244 Gentamycin 90, 225, 231 Geotrichum 176 candidum 40, 176 Ghara 11 Gharial see Gavialis gangeticus Giardia sp. 190, 191 Giemsas stain 168 Gingivae 63, 76, 176, 179, 182 Gingivitis 218, 249250 Glassy teeth 63, 148, 212, 249, 273 Glaucoma 247 Globulin 48, 49 Glomerular ltration Glossina palpalis 191, 205 Glossitis 250 Glottis 12, 13 Glucose 48, 49, 91, 99 Gnathostoma procyonis 197, 199, 274 Goezia gavialidis 193 holmesi 193 lacerticola 193 Goitre 276 Gonads 1819, 79 cysts 266 Goussia sp. 183, 184, 186, 187 Gout 41, 79, 217, 224, 225, 226, 230233, 264, 273, 283 congenital 155, 231 Granuloma 95, 170, 176, 178, 179, 182, 203, 229, 241, 242, 244, 250, 254, 260, 262, 264, 268, 271, 283 Greasy skin 178, 243244, 250 Griphobilharzia amoena 202, 265, 268, 271 Growth 3334, 45, 105, 112, 117, 147, 158, 203, 211, 234 hormone 102 promoter 101, 102 Gular gland see Skin glands Gular valve 11, 55, 63, 76, 77, 87, 250251, 270 Gynecophoric chamber 269

Handling 116, 137, 138, 147, 163, 227, 247, 282 Harmotrema nicollii 201 rudolphii 201 Hartwichia rousseloti 193 Hatching 103, 107 Hearing 44 Heart 77, 82, 86, 284 anatomy 22 ectopic 155 rate 43, 87 septal defect 270 stroke volume 43 surgery 9697 Heating 104105, 109111 Heavy metals 130, 221223 Helobdella sp. 203 Hepatitis 161, 167, 175, 229, 259261 Hepatozoon 188190, 204, 262, 269 brasiliensis 190 caimani 190, 205 crocodilinorum 190 hankini 190 pettiti 190, 205 sheppardi 190 Hernia, diaphragmatic 144 Herpetodiplostomum caimanicola 201 Heterophils 25, 67, 274 Hibernation 177, 281 Hide boards 109, 115, 227, 242, 290 High walk see Walking Hirudinaria manillensis 203, 204 Histopathology sampling 83, 84 Hookworm 197, 199200 Humane killing 76, 124, 138 Humidity 105, 106 Hunting see Foraging Hybridization see Cross breeding Hydrocephalus 153 Hydropericardium 148, 167, 221 Hydrophobia 281, 283, 290 Hydroxidione 94 Hyperglycaemia 91 Hyperkeratosis 233, 250 Hyperparathyroidism see Parathyroidosis Hyperthermia 93 Hypervitaminosis D 225, 265 Hypocalcaemia 212, 215, 225 Hypoglycaemia 47, 91, 138, 148, 282 Hypoproteinaemia 148, 221 Hypothermia 44, 92, 96, 97

Haematology 6769, 234 Haementeria lutzi 203 Haemogregarines see Hepatozoon Haffnia alvei 38 Halophilic bacteria 128 Halothane 92, 95

Icing 44, 56 Identication 61, 7475 Ileum 17, 37 ulcers 267

330

Index

Immobilization 70, 92, 138, 166, 215, 265, 282, 283, 286, 290 Immunoglobulin 45 Immunity 4546, 74, 126, 136, 145, 157, 164, 175, 176, 183, 207, 219, 226, 227, 229, 234, 236, 240, 252, 271, 281, 282 Imprinting 53 Inclusion bodies 157, 158, 159, 161, 240, 259, 272 Incubation 102107, 136, 140, 148, 149, 234 period 43 room 104 temperature see Temperature, incubation Indo-Pacic crocodile see Crocodylus porosus Infertility 121 Inammation 46, 283 Inuenza C virus 163 Injection 8789 Injury 46, 76, 117, 138, 140, 149, 153, 241242, 246, 247, 250, 258, 265, 269, 273, 284287 Inositol 100 Insulin 47, 91 Intestine 93, 200 anatomy 1617 ora see Flora mycosis 179 occlusion 146, 164, 234, 256, 258, 284 Iodine 99, 100, 171 Iron 48, 50, 99, 100, 222 Islets of Langerhans 22 Isosospora 183 jacarei 183, 184 wilkei 183, 184 Ivermectin 89, 209, 225

Jaw malformations 153 Jejunum 16, 37 Johnstons crocodile see Crocodylus johnsoni Jumping 36

Kanamycin 90 Keratoconjunctivitis 246 Ketaconazole 90, 241, 242, 282 Ketamine 71, 92, 93, 95 Kidney 18, 79, 199, 202, 203, 217, 221, 223, 229, 230, 231, 263265, 283 aplasia 155, 231, 264 hyaline degeneration 225, 264265 parasites 265 Kidney:heart ratio 86 Klebsiella 174 oxytoca 38, 39, 174 pneumoniae 38 Kocuria varians 39 Kurthia gibsonii 39 Kyphoscoliosis see Scoliosis

Labyrinth see Ear Lactate 49 Lactobacillus sp. 39 Laparoscopy 9294 Laparotomy 94 Larynx 77, 96 Laurobolin see Anabolic steroids Lead 221223 Leeches 67, 189, 196, 203205, 241 Leg weakness 212, 268, 272, 290 Leiperia 205 australiensis 207 cincinnalis 207, 268, 271 Leishmania sp. 190191 Lethal injection 76 Leucocyte counts 6769 Lidocaine 95 Light 111, 112, 148, 282 Lignocaine 92 Limb duplication 151, 273 missing 273 Limnothrissa miodon lake sardine 119, 193 Lipids see Fat Lipoma 284 Lithophagy 36, 95, 254, 281, 290 Liver 17, 79, 82, 182, 189, 198, 221, 222, 223, 226, 229, 234 cirrhosis 254, 261 fatty degeneration 226, 261 parasites 261262 Locomotion 35 Longevity 3435 Lung 77, 167, 176, 177, 178, 182, 202, 203, 205, 207208 anatomy 12, emphysema 262 haemorrhage 208, 272 Lymph hearts 24 nodes 24, 46, 82 vessels 24 Lymphocytes 24, 25, 45, 57, 190, 229, 259, 266, 274 Lymphosarcoma 284

M99 see Etorphine Magnesium 48, 49, 50 sulphate 253 Maladaptation 235 Malnutrition 136, 148, 226 Manganese 99, 222 Meat 51, 128, 221, 223, 224, 225, 245, 274 cooking hints 133 medicinal use 132 Mebendazol 90 Medication 8691 Medicinal uses 131

Index

331

Melanosuchus niger 5, 28, 192, 193, 201, 207 Menadione 100 Meningitis 167, 246, 267, 290 Mercury 221223 Mesodiplostomum gladiolum 201 Mesothelioma 284 Metabolic rate 34, 40, 43, 91, 98, 105, 112, 148 Metarhizium anisopliae 176, 178 Metronidazole 148, 283 Microchips 75 Micrococcus kristinae 130 luteus 39, 130 nishinomiyaensis 130 roseus 130 sedentarius 130 Microlariae 198, 269 Micromelia 151 Microphthalmia 153 Micropleura vazii 197 vivpara 197 Minerals 99, 136 premix 99100, 121, 241, 245 trace 99 Mirex 223 Mites 205 Molybdenum 222, 223 Monocytes 26, 190 Monogenetic trematodes 200, 209210 Monophthalmia 152 Monorhiny 153 Moraxella sp. 38, 130 Morelets crocodile see Crocodylus moreletii Morganella 37 morgani 38, 174 Morphometry 85, 269, 270 Mosquitos 159, 188, 191, 198, 205 MS222 see Tricaine Mucor 177, 178, 181 circinelloides 176, 177, 179, 252 Mugger see Crocodylus palustris Multicaecum agile 193 Muscle 221, 222, 223, 231 anatomy 10 respiratory 12 tail 10 calcication 220, 225 degeneration 130, 219220 lesions 176, 182 ossication 225 parasites 197, 199, 274 Mycobacterial abscess 250 Mycobacteriosis 73, 130, 170171, 182, 244, 250, 262 Mycobacterium avium 74, 170

bovis 130, 170 fortuitum 170 marinum 170 terrae 170 triviale 170 tuberculosis 130, 170 ulcerans 170 Mycoplasma 74, 117 alligatoris 167, 267, 269 crocodyli 91, 167 Mycoplasmosis 167, 246, 247, 271, 273, 287 Mycotoxins 226, 261, 267 Myocarditis 167, 175, 229, 269 Myositis 274, 290 Myxobolus sp. 210

Nandrolone see Anabolic steroids Navel 33 infection see Omphalitis Necrosis 46, 158, 168, 277 Nematodes 192200 Neodiplostomum 201 crocodilorum 201 gavialis 201 Neoparadiplostomum kafuensis 201 magnitesticulatum 201 Neoplasms 283284 Neostigmine 71 Neostrigea africana 201 leiperi 201 Nephritis 230 interstitial 271 Nephrocephalus sessilis 201 Nesting 42, 54, 102, 119 substrates 102 Newcastle disease 162163 New Guinea crocodile see Crocodylus novaeguineae Niacin 100 Nickel 222, 223 Nictitating membrane 28, 153, 169, 245, 247 Nile crocodile see Crocodylus niloticus Nutrition 98102, 230, 234, 241 state of 6062, 86 Nutritional bone disease 63, 211216, 249, 268, 272

Odneriotrema incommodum 200, 203 microcephala 200 Oedema 46, 167, 172, 175, 217, 221, 229, 244 Oesophagus 14, 78, 87, 95, 200 stenosis 155 Oistosomum caduceus 201 Olfaction 44

332

Index

Omphalitis 142, 143 Oophoritis 265 Opacication cornea 247 3rd eyelid 247 Ophthalmia 246, 247 Opisthotonus see Star gazing Orchitis 266 Organ minerals 49, 222 Orinoco crocodile see Crocodylus intermedius Ortleppascaris alata 193 antipini 193 nigra 193 Osmoregulation 42 Osteoderms 9, 44, 71 Osteodystrophy 211, 273 Osteolaemus tetraspis 3, 16, 18, 28, 35, 36, 38, 3940, 52, 56, 82, 89, 98, 130, 174, 176, 187, 190, 193, 195, 198, 199, 202, 203, 207, 208, 247, 252, 254, 255, 259, 261, 263, 269, 274, 275, 276, 277 Osteomalacia 136, 148, 211, 249, 268, 272273, 275, 290, 291 Osteoporosis 136, 211, 212, 249, 273, 275 Oswaldolaria bacillaris 197, 198, 205 kanbaya 197 medemi 198 versterae 197, 198 Ovary 18, 94, 266 haemorrhage 266 Overcrowding 137, 147, 163, 227, 234, 236, 237, 239, 245, 280 Overfeeding 245 Overheating 4445, 108, 111, 112, 134, 137, 147, 164, 227, 245, 280, 282, 289 Overstocking see Overcrowding Oviduct 19, 79, 94, 140, 153, 265 rupture 120 Ovulation 42, 123, 140, 141, 153, 265 Oxfendazol 90, 194 Oxygen consumption 40, 103, 105 Oxytetracyclin see Tetracycline

Pachypsolus constrictus 201 sclerops 201 Paecilomyces 40, 177 aviotti 141 farinosus 177, 178 lilacinus 141 Pain 92, 138, 290 Palaeosuchus palpebrosus 5, 28, 52, 71 trigonatus 5, 28, 52, 71, 198

Pancreas 16, 17, 18, 22, 79, 234, 259 Pancreatic involution 259 Pancreatitis 259 Panophthalmitis 247 Pansteatitis see Steatitis Pantothenic acid 100 Papilloma 283 Paradiplostomum abbreviatum 201 Paralysis 172, 212, 218, 219, 224, 225, 231, 267, 268, 273 Paramyxovirus 162163, 228, 246, 266 Parasitaemia 189 Parasites gastric 79 sampling 82, 85 Parathyroids 22, 77, 211, 212, 275 cysts 212 Parathyroidosis 211, 275 Paratrichosoma 195196, 241 crocodylus 195 recurvum 195 Parental care 53 Pasteurella 38 haemolytica 38 multocida 174 Pectoral girdle 7 Pellets 101, 118, 194, 227 Pelvic girdle 8, 77 Penicillin 90, 91, 171 Penicillium 38, 40, 177 felucanum 141 lilacinum 177, 178 oxalicum 177 Penis 19, 21, 66, 70, 132, 266 Pentobarbital 71, 73, 93, 95, 96 Pentamethylene tetrazol 93 Pentastomes 117, 205209, 271, 272 sampling 85, 271 Peptococcus magnus 37 prevotii 37 Pericarditis 97, 175, 229, 269 Periocular abscess 247 Peritonitis 120, 140, 144, 254, 265, 284 Pesticides 223224 Pharmacokinetics 91 Pharyngitis 270271 Phenylbutazone 226, 231 Phenylcyclidine 71, 72, 73, 92, 94 Philippine crocodile see Crocodylus mindorensis Philobdella gracilis 203 Phoma sp. 40 Phosphorus 100, 136, 148, 211, 272 blood/serum 48, 49 urine 50 Phthisis bulbi 247 Physical restraint 5760

Index

333

Pigmentation 9 Piling 114115, 242, 245, 290 Piperazine 90, 194 Pithing 125, 138 Pituitary 21 Placobdella multilineata 67, 204, 205 papillifera 204 Placobdelloides multistriatus 204 Plagiorchid ukes 202 Planococcus sp. 174 Plasma minerals 49, 50 Plasmodium sp. 188 Plerocercoids see Cestode larvae Pneumonia 167, 175, 271 foreign body 272 fungal 271, 272 Pole syringe 70, 89 Polyacanthorhynchus rhopalorhynchus 199 Polyarteritis see Arteritis Polyarthritis 164, 167, 172, 175, 287 Polychlorinated hydrocarbons 130, 223, 266 Polycotyle ornata 201 Polydactyly 151, 273 Polymerase chain reaction (PCR) 170 Polymorphus mutabilis 199 Polyp 95 Polyserositis 167, 175, 229 Poor dental mineralization see Glassy teeth Potassium 48, 49, 50 Pox lesions 76, 158, 159 virus 157, 288 caiman 74, 117, 157158, 240, 250 crocodile 74, 90, 117, 158159, 236, 240, 242, 246, 250 Pre-release screening 7374 Probenecid 226, 231 Probiotics 227 Procaine 92, 93 Proctocaecum dorsale 201 Progarnia 188, 190, 269 archosauriae 190 Prolapse of the uterus 215, 265 Prolectithidiplostomum cavum 201 constrictum 201 Prostrigea arcuata 201 Protein 99, 101, 129, 230 blood/serum 48, 49, 50 Proterodiplostomum breve 201 globulare 201 longum 201 medusae 201 tumidilum 201

Proteus 37, 141, 174 mirabilis 38, 39 rettgeri 253 vulgaris 38, 39 Providencia 37 rettgeri 39, 174 , 246, 267 Pseudocrocodilicola americana 202 georgiana 202 Pseudomonas 174, 227 acidivorans 130 aeruginosa 141, 142, 174 cepacia 38 uorescens 38 maltophila 38, 130 pickettii 38 putida 174 Pseudoneodiplostomum 202 acetabulata 202 bifurcatum 202 dollfusi 202 siamense 202 thomasi 202 Pseudotelorchis caimanis 202 yacarei 202 Pseudotumour see Fibriscess Pus 46, 287 Pyelonephritis 203, 231, 263264 Pyloric antrum 14, 79 Pyridoxine 100

Radiography 64 Radionuclides 224 Rana catesbiana 193 Rana sphenocephala 193 Rats see Rodents Rearing 107112 Rectal examination 70 Rectum 17 Red blood cells see Erythrocytes Red heat 128 Regeneration 249, 286 Regurgitation 37, 95, 253, 254 Renal portal system 24 Renivermis crocodyli 202, 265 Reproductive performance 101102, 221, 224 Respiratory rate 40, 41 Respiratory tract, anatomy 11 Restraint 5760, 137, 138, 279 Retrobulbar abscess 247 Rhabditids 198, 261 Rhinitis 237, 245, 246, 266, 270 Rhinopharyngitis 271 Rhodotorula rubra 38 Riboavin 100

334

Index

Ribs 77, 126 abdominal 7 cervical 7 thoracic 7, 8 Rickets 211 Rodenticides 219, 224, 269 Rodents 109, 111, 118, 188, 197, 228 Round cell tumour 283 Roundworms 117, 192200 Rubber jaws 63, 148, 212 Running 9, 36 Runting 34, 67, 85, 147, 161, 186, 191, 194, 221, 226, 234236, 269, 281

Saffan see Alphaxolone/alphadolone Salicylates 226, 231 Salmonella arizona 142, 166 choleraesuis 164, 165 enteritidis 164, 165 serovars 39, 130, 164, 165166 typhimurium 164, 165, 166 Salmonellae 126, 129, 130, 227, 245, 256 Salmonellosis 87, 91, 164, 234 Salpingitis 265 Salt 41, 90, 204, 205, 253, 283 glands 14, 4142 tolerance 4142 Scapula 7 Schneiders dwarf caiman see Palaeosuchus trigonatus Scoline see Succinylcholine Scoliosis 149, 212 Scratches see Skin Sebekia acuminata 207 cesarisi 207 divestei 207 indica 207 johnstoni 207 jubini 207, 271 microhamus 207 mississippiensis 207 multiannulata 207 novaeguineae 207 okavangoensis 207 oxycephala 208 purdiae 207 samboni 207 trinitatis 207 wedli 207 Selenium 50, 99, 100, 219, 220, 222, 274 Sela porosus 207 Seminal groove 19, 66, 123 Seminoma 283 Sensory pits 5, 6

Septicaemia 46, 79, 87, 97, 126, 129, 130, 137, 138, 143, 147, 163, 164, 167, 170, 172, 173175, 208, 225, 228229, 230, 231, 244, 245, 248, 250, 252, 259, 260, 262, 263, 265, 266, 267, 269, 270, 271, 273, 281, 282, 285, 287, 288 Serine 231 Sernylan see Phenylcyclidine Serratia 37, 174 liquefaciens 174 marscescens 38, 174 odorifera 38, 39 Serum biochemistry 4750 Sex differentiation 3, 42, 105 Sex hormones 122 Sexing 70 Sexual behaviour 54 Shock 91 Siamese crocodile see Crocodylus siamensis Siren lacertina 193 Skeleton 7 Skin 240245 abrasions 76, 135, 177, 178, 242 anatomy 8 discolouration 174, 221, 229, 237, 240 erosion 221, 237 glands 9, 44 dorsal 9 gular 9 paracloacal 9 secreta 52 lesions 176, 177, 195196, 204, 236, 239 necrosis 244 pitting 245 puncture 241, 242 quality 244245 reex 92 scratches 114, 236, 241, 245, 290 ulcers 76, 173, 237, 244 wounds 242 Skinning 124, 126128 Skull deformities 149, 152153 Slaughter 123133, 138, 245 Sliding 36, 135, 242 Snake tongs 5960, 116, 137 Social interactions 54 Sodium 48, 49, 50 Solenopsis 223, 246 invicta 224 Somatostatin 15 Sparganosis see Cestode larvae Spectacled caiman see Caiman crocodilus Sperm 140 collection 66, 123 Spina bida 151 Spinal cord 27, 8082, 89, 124, 125, 133, 138, 212 compression 89 Spirometra erinacei 203

Index

335

Spleen 24, 45, 79, 182, 183 Spleen:heart ratio 86, 87, 270 Splenomegaly 45, 79, 175, 229, 270 Squamous metaplasia 217, 233, 264 Staphylococcus 37, 38, 174 aureus 129, 174 capitis 130 chromogenes 39 epidermidis 39, 130 hominis 130 saprophyticus 130 xylosus 39 Star gazing 268, 289 Starch 99 Steatitis 100, 208, 219, 244, 259, 257 Steatotheca see Fat body Steatothecitis 262263 Stephanoprora jacaretinga 202 ornata 202 Sterility 120 Sternum 7, 287 Stocking density 33, 54, 113, 116117, 134, 137, 235, 280, 284 Stomach 79, 87, 231 anatomy 1416 contents 36, 79, 98 collection 6667 contractions 101 foreign bodies 79, 95, 254255, 263 mycosis 179 pH 36 secretions 36 ulcers 79, 176, 194, 229, 237, 251252, 269 Stomatitis 249250 Streptococcus 37, 174 equisimilis 130 faecium 130 salivarius 39 Streptomyces sp. 39 Streptomycin 224, 225, 231 Stress 33, 34, 37, 44, 47, 5253, 54, 57, 67, 70, 74, 92, 95, 97, 101, 108, 109, 112, 115, 117, 121, 122, 125126, 130, 134, 136, 137, 138, 140, 145, 147, 148, 157, 158, 159, 161, 163, 164, 166, 167, 170, 171, 172, 173, 175, 176, 177, 178, 181, 182, 190, 208, 209, 218, 225, 226, 227, 228, 229, 230, 234, 235, 236, 240, 244, 245, 248, 251, 259, 265, 269, 270, 271, 275, 276277, 278282, 283, 287, 288, 289, 290 pre-slaughter 123, 125, 129, 245 Stressor 137, 164, 166 Strontium 222, 223 Stunning gun see Captive bolt gun Styrofoam 104, 109, 126 Substance depletion 281

Subtriquetra 205, 271 megacephala 207 rileyi 207 shipleyi 207 subtriquetra 207 Succinylcholine 70, 71, 72, 73 Sucostrin see Succinlylcholine Suffocation 114 Sulphachloropyrazine 90, 188 Superstition 131 Supertemporal fossae 7, 62, 76, 125 Surgery 91, 9297, 287, 288 Suxathonium 72, 73 Swimming 35, 135, 219, 268 Syncephalastrum sp. 177 Syndactyly 151

Tagging 7475 Tail deformities 149151 Taillessness 149151, 265, 291 Tapeworm see Cestodes Taurine 102 Teeth 13, 62, 63, 76, 204, 212, 241, 247249, 273 Temperature body 34, 36, 40, 41, 43, 4445, 56, 88, 101, 105, 112, 130, 134, 137, 227, 230, 281, 288, 289 tolerated minimum 44 environmental 33, 3536, 44, 91, 99, 101, 108, 109, 134, 148, 173, 174, 177, 178, 182, 226, 227, 228, 229, 231, 233, 234, 235, 236, 237, 240, 241, 244, 289 uctuations 106, 109, 120, 121, 142, 148, 161, 163, 164, 166, 227, 232, 234, 241, 244, 280, 282 incubation 33, 42, 43, 45, 54, 104, 105106, 149, 151, 153, 154 rearing 109110, 111112 Terranova crocodili 193 lanceolata 193 Territoriality 54, 284 Testis 19 Tetany 290 Tetracycline 34, 90, 101, 102, 147, 167, 169, 173, 247, 254 Thallium 222 Thermogradient 44, 55, 109, 112, 120, 134, 135, 136, 234, 289 Thermoregulation 43, 4445, 5556, 120, 134, 137, 173, 231, 280, 289 Thiabendazol 90 Thiaminase 217 Thiamin 100 deciency 217218, 268, 269, 289 Thiopental 92, 93

336

Index

Third eye lid see Nictitating membrane Thrombocytes 24, 190 Thymus 2122, 24, 45, 77, 274275 cyst 275 necrosis 274275 Thyroid 22, 77, 275276 cysts 275, 284 Thyroxine 47, 49, 102 Tibial puncture 89 Ticks 205 Tiletamine see Zoletil Timoniella absita 202 Tin 222 Toltrazuril 90, 188 Tomistoma schlegelii 3, 9, 28, 48, 223, 231, 273 Tongue 13, 63, 76, 77, 179, 182, 217 Tonsils 11, 12, 24, 251, 270 Tooth replacement 13, 247 Toothlessness 247 Torsio intestinalis 258, 259 Torticollis 254 Torulopsis sp. 38 Toxaemia 143 Transovarial infection 140, 141, 160, 188 Transport 121, 126, 137138, 175, 177, 229, 230, 252, 279, 281, 282, 283 Trauma see Injury Trematodes 117, 192, 200203, 264 Triatoma infestans 205 Tricaine 71, 72, 73, 92, 94 Trichinella 197, 274 spiralis 197 Trichinellosis 130, 196 Trichoderma sp. 38, 40, 177 Trichomonas 190 prowazeki 190 Trichophyton sp. 177 Trichosporon 177, 179, 182 beigelii 38, 40 capitatum 40 cutaneum 177 Triglyceride 48 Trispiculascaris asymmetrica 193 trispiculascaris 193 Trypanosoma 191192, 269 cecili 192 grayi 191, 192, 205 Trypanosomes see Trypanosoma Tuberculosis see Mycobacteriosis Tubocurarine 93 Twins 151, 153154 Tympanic membrane see Ear Typhlophorus lamellaris 193 spratti 193

Ultrasonography 64 Urea 41, 48, 49 Uric acid 41, 48, 49, 50, 225, 230 Urine 41, 121, 135 biochemistry 4849 collection 65 pH 50 retention 212 Uterus 19, 42, 70, 265 Uveitis 247

Vaccine 90, 157, 159, 161, 166, 167 Valium see Diazepam Vanadium 222 Vasoconstriction 43 Vermiculite 104, 106107, 141 Viadril see Hydroxidione Vinegar 254 Virginiamycin 101, 102, 147 Virus isolation 83, 157 particles 83, 157, 158, 159, 160, 162, 163 Vitamins 101, 121, 136, 149 A 100, 216217, 230, 231, 233, 264 B 100, 217218, 226, 254, 261 C 100, 147, 170, 218219, 229, 250, 281, 282 D 100, 211, 225, 265 E 50, 100, 121, 218, 219221, 274 K 100, 266, 269 premix 99100, 241, 245 Vitello-intestinal duct 32, 142, 143 Vocalization 56

Walking 9, 36, 135, 242 Warfarin see Rodenticides Warts 283 White claws 9, 273, 274 White muscle disease 219220, 274, 288, 290 White nose 229, 237239, 241 Winter sores 173, 236237, 240, 241, 244

Xylazine 71 Xylocaine 92

Yawning 55 Yersinia enterocolitica 38 Yolk-sac anatomy 3233, 142 excision 96, 144 hydropic 144 infection 142, 148, 234 resorption 32, 142, 148, 234

Index

337

retention 142, 143145, 257 rupture 143 Zenkers degeneration see White muscle disease ZiehlNeelsen stain 170 Zilka 125 Zinc 99, 121, 281

bacitracin 100, 102 deciency 221 plasma 50, 223 sulphate 173 Zolazepam see Zoletil Zoletil 72, 73