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Hydrobiologia 403: 153193, 1999. 1999 Kluwer Academic Publishers. Printed in the Netherlands.

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Barbels and barbel-like tentacular structures in sub-mammalian vertebrates: a review


Harold Fox
Department of Biology, University College, Gower Street, London, WC1E 6BT, U.K.
Received 8 March 1999

Key words: barbels, tentacles, shes, amphibians, reptiles, structure, function, phylogeny

Abstract The following account is a synthesis of current knowledge on the barbels/tentacles of an array of submammalian forms and for the rst time compares and contrasts their structure and function. In addition, the extensive background information on the homology and phylogeny of these structures is reviewed and evaluated.

Introduction Tentacles of vertebrates considered in the present work are arbitrarily dened as, those specic elongate structures that arise independently from the head or branchial region, covered with skin and in some cases supported within by a cartilaginous (or bony) skeleton, innervated by branches of the cranial nerves, and in shes usually having sensory components, the taste buds, in the epidermis. Among shes, elongate pectoral and pelvic n rays (see Sterba, 1962; Kotrschal et al., 1984; Finger, 1988) and illicia, that are modied dorsal n rays with luminescent photophores (Bertin, 1958), though sensory in function are not strictly tentacles as so dened: however they are considered, albeit briey, where they have some relevance to barbels. Fishes in particular, a number of amphibians and some few reptiles have tentacles in the head region. In shes, these are the conspicuous barbels and the lesser developed oral papillae and orbital cirrhi. Among amphibians, larvae of some urodeles possess balancers on each side of the branchial region and those of a few anurans have elongate tentacles, or whiskers, near the mouth. Adult apodans have laterally disposed tentacles on the head. Some chelonians and the aquatic snake Erpeton tentaculatum among the reptiles possess tentacle-like

extensions in the head region; structures comparable to those of the other groups. The multicellular epidermis of shes includes many highly specialized cell types, including unicellular and multicellular glandular components (Whitear, 1971, 1986; Fox et al., 1980). Among these are electroreceptors (Zakon, 1988) and lateral-line neuromasts (see among others Coombs et al., 1989; Webb, 1989), organs not present in barbels, and the gustatory system that is (Kapoor et al., 1975; Reutter, 1986). The skin is also extensively innervated by free nerve endings (Whitear, 1983, 1986). Many shes, especially teleosts, have barbels usually replete with sensory buds, the Endknospen of classical German workers (Merkel, 1860; see Wright, 1884; Bateson, 1890), hitherto believed to serve mainly a taste function (Herrick, 1903): the lips are also well supplied with taste buds. Larval amphibian body skin of Rana temporaria, among other cellular components, uniquely has unicellular chemosensory cells, the Stiftchenzellen (Whitear, 1976). All have lateral-line neuromasts (Morup-Jorgensen & Flock, 1973); Fritzsch, 1981, 1988). Electroreceptors occur in body skin of salamander and apodan larvae (Fritzsch & Wahnstaffe, 1983; Fritzsch et al., 1985), the gustatory organs conned to the oral cavity in all amphibians (Zuwala & Jakubowski, 1991).

154 Gustatory, lateral-line and electroreceptor sensory organs are lacking in reptilian skin, incuding that of the tentacles, but epidermal multicellular structures subserve mechanoreception, thermoreception and possibly sensitivity to humidity (Landmann, 1975; Maclean, 1986; Ananjeva et al., 1991). Despite the immense literature on the subject of vertebrate tentacles, especially barbels of shes, information is singularly lacking or limited, on a variety of features, including an understanding of their functional mechanisms and the specic contribution of different cell components in sh barbels to their functional activity. Even less is known, with any degree of certainty, about tentacle function in amphibians, and chelonians and Erpeton among the reptiles. The following account, therefore, is a synthesis of current knowledge on the barbels/tentacles of these submammalian forms and for the rst time compares and contrasts their structure and function, In addition, the extensive background information on the homology and phylogeny of these structures is reviewed and evaluated. Barbels in shes Distribution and form (see Table 1) Among the phylogenetically lower groups of chordates Amphioxus, of the Cephalochordata has buccal cirrhi. Among the Hemichordata Cephalodiscus has foursix pairs of ciliated tentacles near the mouth; Rhabdopleura likewise has two lateral arms in the head region, each bearing two rows of cilia associated with nerves (Dilly, 1971). These structures play a role in the transport of food particles to the mouth. Barbels are not present in the Petromyzontiformes. However, among the Myxiniformes, in the Myxinidae, Myxine glutinosa and Eptatretus burgeri have four pairs of oral tentacles (Patzner et al., 1977), those of Myxine innervated by tbe trigeminal ramus ophthalmicus profundus and rami maxillaris and mandibularis nerves (Pollard, 1895). The lamprey Geotria australis has several small and two large papillae around the mouth, believed to be encapsulated mechanoreceptors that enable the animal to locate and attach itself to host shes or other surfaces (Cook et al., 1990). Oral cirrhi, under the hood of the ammocoete Lampetra uviatilis, contain oligovillous and Merkel cells (Whitear & Lane, 1983). Among the elasmobranchs in the Squaliformes there are barbeled forms, for example in Pristiophorus
Figures 13. Figure 1. Frontal view of the head of the catsh Corydoras arcuata showing the three pairs of barbels. Figure 2. Low power scanning electronmicrograph (SEM) of two maxillary and one mental barbel (arrowed), showing taste buds at the surface. (X 36). Figure 3. Higher power SEM of a mental barbel with abundant taste buds at the surface. (X 190). (From W, K. Ovalle & S. L. Shinn 1977, Cell Tiss. Res. 178).

japonicus and Pliotrema. Likewise in the Squatinidae, the angel sharks, the nostrils terminate in anterior barbel like processes. Carcharhiniformes also include forms with barbels leading from the nostril region and reaching the mouth. Among the Acipenseriformes of the Chondrostei, all members of the Acipenseridae, for example Acipenser sturio (a mud-feeding form) among others (Meng, 1923), have a pair of short barbels on each side of the snout in front of the mouth. Polyodon spathulus and Psephurus gladius, of the Polyodontidae, have minute barbels on the snout (Nelson, 1984). Barbels have a widespread distribution among the teleosts (see Figure 4), though indeed members of many orders do not possess them. They are also variable even within the different families of orders

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Table 1. List of orders and families of chordates, including Hemichordata, Cephalochordata, Cyclostomata, Elasmobranchii, Chondrostei and Teleostei that provides a general indication of the distribution of barbels (tentacles and cirrhi) in shes. Among the ostariophysans, maxillary barbels are present in many cypriniforms and in all siluroids. Barbels are missing in characiforms, gymnotoids and the gonorynchiforms. Likewise within families of different orders of teleosts, barbels may occur in some species and not in others, and they may be present or missing even in the different subspecies. (Compiled from among others, Sterba, 1962; Greenwood et al., 1966; Norman, 1975; Fink & Fink, 1981; Nelson, 1984; Collette et al., 1984; Fahay & Markle, 1984; Maisey, 1984; Howes, 1991). Sub-phylum: Hemichordata Class: Pleurobranchia Order: Rhabdopleuriformes Rhabdopleura 2 lateral tentacle-like ciliated arms in the head region Sub-phylum: Cephalochordata Order: Amphioxiformes Amphioxus cirrhi situated around the mouth Sub-phylum Vertebrata (Craniata) Superclass: Cyclostomata (Agnatha) Order: Myxiniformes Families Myxinidae: (hagshes); 4 pairs of oral barbels Petromyzontidae (lampreys); papillae around the mouth in Geotria australis Subclass: Elasmobranchii Order: Squaliformes Families Pristiophoridae: (saw sharks); 1 pair of long barbels, those of Pristiophorus japonicus are up to 50 mm long Squatinidae: (angel sharks); nostrils terminal with barbels on the anterior margin Orectolobiformes Family Orectolobidae: (carpet or nurse sharks); 1 pair of well developed barbels from the nostrils Infraclass: Chondrostei Order: Acipenseriformes Families Acipenseridae: (sturgeons); 2 pairs of barbels in front of the mouth Polyodontidae: (paddle shes); minute barbels on the snout in Polyodon spathula and Psephurus gladius Subclass: Brachiopterygii Order: Polypteriformes Family Polypteridae: (bichirs): tentacle-like structures associated with the nostrils in Polypterus and Erpetoichthys SubDivision Teleostei Order: Osteoglossiformes Family Notopteridae: (knife shes); small nasal tentacles Continued on p. 156

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Table 1. Continued Superorder: Ostariophysi Order: Cypriniformes Families Cyprinidae: 2 barbels on each side of the mouth Cyprinus carpio: Barbus vulgaris etc.). C. carpio has the front pair of barbels about 4 times as long as the pair behind. There are also very long barbels in Esomus lineatus and E. dancrica: In E. dancrica 85 mm long, the barbels are almost half the length of the sh. There is a barbel on each side of the head in Gobio gobio Cobatididae: 36 pairs of well developed barbels; for example 10 barbels in Misgurnus fossilis and M. anguillicaudatus, the 4 on the lower jaw much shorter than the other 6 Subfamily Cobitidinae: 1 pair of rostral barbels Subfamily Botiinae : 3 or more pairs of rostral barbels Order: Siluriformes Families Ageneiosidae: (bottlenose or barbel-less catshes); only maxillary barbels present, sometimes even these are rudimentary Akysidae: (stream catshes); barbels present Amblycipitidae: (torrent catshes); 4 pairs of barbels Amphiliidae: (loach catshes); 3 pairs of barbels Ariidae: (sea catshes; usually 3 pairs of barbels; nasal barbels missing Aspredinidae: (banjo catshes); barbels present Astroblepidae: small barbels present Auchenipteridae: 3 pairs of barbels (except one species with 1 pair): the maxillary barbels are the longest Bagridae: (bagrid catshes); 4 pairs of well developed barbels Callichthyidae: (callichthyid armoured catshes); barbel-like structures around the mouth Cetopsidae: (whale-like catshes); 3 pairs of barbels; nasal barbels missing Chacidae: (squarehead or angler catshes); barbels present. Chaca uses its maxillary barbels to lure prey closer to its mouth Clariidae: (air-breathing catshes); 4 pairs of long barbels Cranoglanididae: (armoured catshes); 4 pairs of barbels Diplomystidae: (diplostomid catshes); only maxillary barbels present Doradidae: (thorny catshes); 3 pairs of barbels; nasals missing Helogenidae: longish pair of chin barbels Heteropneustidae (air-sac cattishes); 4 pairs of barbels (Saccobranchidae): Hypophthalmidae: (low-eye catshes); 3 pairs of barbels Ictaluridae 4 pairs of barbels on head: 2 nasals, 2 maxillary and 2 (Ameiuridae): pairs on the chin Malapteruridae: (electric catshes); barbels present Mochokidae: (squeakers or upside-down catshes-; barbel-like fringed (Synodontidae) extensions from the front of the head. Barbels well developed. In Synodontis sp. 100 mm long, barbel up to 40 mm long extending posteriorly Olyridae: 4 pairs of barbels Pangasiidae: usually 2 pairs of barbels; nasal barbels missing; 1 pair of chin barbels Pimelodidae: (long-whiskered catshes); 3 pairs of moderately long barbels. In some forms, for example Heptapterus mustelinus, the maxillary pair reach the pectoral ns when laid back Plotosidae: (eel-tail catshes); 4 pairs of barbels Continued on p. 157

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Table 1. Continued Schilbidae: Siluridae: Sisoridae: Trichomycteridae (Pygidiidae): (schilbid catshes); 24 pairs of barbels. In Physalia pellucida (African glass catsh) 90 mm long, the 4 pairs of barbels are each 30 mm long 2 pairs of barbels usually present (sisorid catshes); 4 pairs of barbels (pencil or parasitic catshes); generally 2 pairs of maxillary barbels; chin barbels usually absent

Order: Stomiiformes Family Stomiidae: (scaly dragon shes); long barbel on the chin Astronesthidae: (snaggletooths); long barbel present, slightly bulbous at the tip Chauliodontidae: (viper shes); short chin barbel present in some members Idiacanthidae: (black dragon shes); chin barbel only in females Malacosteidae: (loose jaws); chin barbel on most species Melanostomiidae: (scale-less black dragon shes); most species with barbel on the chin (All the above are now considered to be members of the family Stomildae; see Fink, 1984; Kawaguchi and Moser, 1984); the barbeled forms believed to be a monophyletic group (Fink, 1984) Order Myctophiformes Family Myctophidae: (lantern shes); Diogenichthys atlanticus has a chin barbel Order: Gadiformes Gadidae: (cods, haddocks); chin barbel usually present. Gadus macrocephalus has 1 pair of barbels on the lower jaw, each slightly longer than the diameter of the eye Lotidae: chin barbel always present Macrouridae chin barbel usually present (Coryphaenoididae): Moridae: (Morid cods); chin barbel present in some species Muraenolepidae: barbel on the lower jaw Phycidae: barbels on the lower jaw and on the snout in some species Order: Ophidiiformes Family Ophidiidae: Subfamily:

(cusk eels) Brotulinae: barbels present on chin and snout. They are missing in the Brotulotaeninae, Neobythitinae and Ophidiinae

Order: Lophiiformes (Angler shes) The rst ray of the spinous dorsal, if present on the head, is transformed into a barbel-like structure, an illicium; a line and bait device to lure prey into the mouth Families Centrophrynidae: Linophrynidae: Lophiidae:

(deep-sea anglers); small hyoid barbels in the young males parasitic on the females. Hyoid barbels in females of Linophryne (goose shes); moveable shing rod device has a ap of esh at the tip, which acts like a ag attracting prey to its large mouth. There are small aps around the lower jaw and on the sides of the head and body. Long laments are present around the mouth in Lophius litulon Continued on p. 158

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Table 1. Continued Order: Beloniformes Family Exocoetidae: (ying shes); many species of Exocoetus have barbels that range in length from short to longer than the body. Exocoetus obtusirostris and E. volitans, however, do not possess barbels Order: Polymixiiformes Family Polymixiidae: (beard shes); 1 pair of hyoid barbels Order: Scorpaeniformes Families Cottidae: barbels present on the head (Cottus, Blepsias) Agonidae: (poachers) Subfamily: Agoninae short chin barbel (Agonus) Order: Perciformes Families Mullidae: Notograptidae: Percophidae: Subfamily: Subfamily: Uranoscopidae: Mastacembelidae:

(goat shes); 2 long chin barbels median barbel on the lower jaw (duck bills); Bempropinae: maxillary barbels in Bemprops Hemerocoetinae: median barbel at tip of snout in some species. Only males of Heterocoetes have a barbel (stargazers); some species with a small tentacle-like lament extending from the oor of the mouth to lure prey. (spiny eels); eshy rostral appendage present particularly in Macrognathus

that possess them. Barbels are most common in the Siluriformes, the catshes (Figures 13). Among ostariophysans, barbels are found in cypriniforms and siluroids but are lacking in characiforms, gymnotoids and Gonorhynchiformes (Fink & Fink, 1981). Among cyprinid cypriniforms they occur in Cyprininae, Gobioninae and Rasborinae; they are lacking or are sporadic in the Leuciscinae, Acheilognathidae, Cultrinae and Alburninae (Howes, 1991). The number of barbels in different forms varies; they may be absent or reach a maximum of four pairs in the subfamily Gobiotinae (Arai, 1982). Many cypriniforms and all siluroids have maxillary barbels; however, they differ in their location and relationship to the cheek skin. Other ostariophysans lack a maxillary barbel. Again, some Eurasian cyprinids have very long barbels, for example Esomus danrica: in others, barbels are variable in their presence (Baranescu & Coad, 1991). In Gadiformes, among the Macrouridae, Fahay & Markle (1984) listed 31 genera: among them, a chin

barbel is present in 23 (three genera had tiny barbels), a chin barbel was present or absent in three genera and absent in ve genera. Likewise, among Beloniformes (Collette et al., 1984), barbels of Exocoetus range in size from short to longer than the entire body. Yet Exoceotus obtusirostris and E. volitans have no barbels, nor do Parexocoetus mento, species of Cypselurus, Prognichthys and Hirundichthys (Kovalevskaya, 1982). Paired barbels develop in Parexocoetus brachypterus and in all species of Cheilopogon, where the barbels are thick and branched. In Cheilopogon cyanopterus, the barbel has two three aps and is longer than the body. Barbels are short in Cheilopogon heterurus doederleini or long in C. unicolor and those of Cheilopogon pinnibarbatus are fringed (Kovalevskaya, 1982). The barbel is single in Cypselurus and Exocoetus monocirrhus. Collette et al., (1984) listed 33 species of Exocoetus, where barbels present in 18 of them. Such barbels may be short,

159 bulb, as well as photophores on the head and anterior trunk. There is also a subocular light organ. Such luminescent organs in barbels have not been described histologically, or by scanning or transmission electromicroscopy, nor are they mentioned in any account of barbel ne structure (vide infra). Reports therefore, of so-called photophores, or other types of bioluminescent structures, in barbels of stomiatoid shes, would need verication and/ or further description. In the Lophoformes (angler shes), some of whose families have barbels or aps around the mouth, it is of interest that the rst n ray of the spinous dorsus, if present on the head, is transformed into a line and bait device, an illicium, to attract prey into the mouth. This structure is of variable length, for example between 3 cm and 36 cm long, in different species of the Antennaridae, where it is particularly pronounced. In the suborder Ceratoitdei, only the females have an in illicium at the tip, with a light organ. In the Gigantidae, the illicium in front of the head is as long or longer than the body: it is also long (and branched) in the Himantolophidae. In the Diceratidae, females are distinguished from other ceratoids by the presence of a second club- shaped cephalic ray, with a distal light organ (see Nelson, 1975; Norman, 1984). Among teleosts, in the Perciformes, cirrhi are found above the eyes, for example among the Blennidae. Hypsoblennius gilberti and H. gentilis and the Hexagrammidae, Oxylebus pictus. The cirrhi are innervated by the facial and trigeminal nerves and a gustatory function is suspected (von Bartheld & Meyer, 1985; see also Sabatese, 1994). Papillae in rows under the head of the gobid sh Paragobiodon echinocephalus, appear to be concerned with chemoreception (Zander, 1970).

Figure 4. Head of Blepsias cirrhosus draciscus with barbels and short projections. mb, mandibular barbel; np, nasal pores; pob, posterior snout barbel; prb, anterior snout barbel; sb, short barbel: sob, supraorbital barbel.

medium or long, fan-like or attened, lamentous or petalous, either paired or single. Among teleosts barbels differ widely in absolute and relative size within and between species. For example barbels of Cyprinus, Tinca, Gobio Barbus and Lota range from 2% tp 6% of body length (RafnPeyloz, 1955). Misgurnus fossilis, 8.522.5 cm long, has barbels 910 mm long (Ducros, 19531954). The Japanese goatsh, Upenoides bensasi, has a chin barbel 20% of its body length and in the Japanese catsh, Plotosus anguillaris, the four pairs of barbels ae 1325 mm long (Sato, 1937a,d). The most impressive barbels occur in the deep-sea stomiatoid shes, where in Ultimostomias mirabilis barbel length is up to 417 mm, probably the longest known and 10.4 the length of the sh (Beebe, 1933) (Figure 5). For further information on barbel size see among others Sato (1937d, 1977a), Sato & Kapoor (1957), Nagar & Mathur (1958) and Singh & Kaoor (1967). The gross structure of barbels of a number of deepsea stomiatoid teleosts was described by Beebe (1933) and Parr (1933). The shes listed had photophores (Bertin, 1958; Herring, 1982) along the body and ve species were reported to have them along the bulbous terminally branched barbels, including the elongate barbels of Ultimostomias mirabiis (Beebe, 1933). Nichol (1967 showed the head of Stomias brevibarbatus to have a mental barbel with a luminescent

Homology and a phylogenetic consideration of barbels A century ago, Pollard (1894) attempted to demonstrate morphological similarities of skeletal (procartilaginous) structures and nerves, in barbels of silurid shes, that could traced back to a Myxine-type ancestral form. Such structures, in Myxine tentacles, were claimed to occur in the oral cirrhi of Ampioxus and believed to be homologous. This view implied that barbels of shes are homologues of the oral cirrhi of Amphioxus the cirrhostomial theory which also embraces ideas on the origin ot the head skeleton.

160 Pollard (1894) believed that the ancestors of Myxine originally possessed at least eight pairs of oral cirrhi, as in Amphioxus, some of which were subsequently lost. Furthermore, the cartilaginous root piece of the maxillary tentacle of Myxine is continuous with the skull and possibly the cranium is an extension of the root piece, which in Myxine protects the auditory organ and in gnathostomes the brain and olfactory organs. Pollards results would lead to the conclusion that all barbels of shes are homologous and of ancient lineage. Indeed, their fairly widespread occurrence and general similarity in structure, function and location would lend support to this view. However, more recent workers doubt the homology and phylogenetic relationships of barbels, at least between the different families of teleosts (vide infra). Likewise, other work on chondrocranial ontogeny (see de Beer, 1950), shows that Pollards cirrhostomial theory should be treated as an imaginative concept mainly of historical interest. Arai (1982) believed that cyprinids with barbels are more primtive than those without them. However, Howes (1991) disagreed on the grounds that more cyprinids lack barbels than possess them and some species with barbels show modication of their nerve distribution and of the maxilla, changes derived from taxa without barbels. Nevertheless, some species show secondary loss of barbels, for example squaliobarbin cyprinids and Barbus and perhaps Carassius, which usually lacks anterior and posterior barbels (Howes, 1991). Likewise, in silurids, where the number of pairs of barbels (in adults) is a useful parameter for recognition of families, in the pangasid Silonia silondia the three pairs of barbels (nasals, maxillary and mandibular) reduce during ontogeny, until nally only a minute pair of maxillary barbels remain (Karamanchandani & Motwani, 1956): in Parasilurus asotus the second pair of mental barbels disappear during development (Atoda, 1935; vide infra (Figures 9ad). Collette et al. (1984) believed that barbels of Exocoetus are derived from paired cutaneous lappets on the lower jaw of needle shes, halfbeaks and primitive ying shes of this group. The most generalised state is of two individual barbels, a view inferred from the ontogeny of two juveniles of Parexocoetus brachypterus brachypterus. The smaller juvenile had a small beak on which two barbels fuse into the single chin barbel of the older juvenile. Thus secondary loss of barbels can be a derived state and presumably it has occurred independently in the three most advanced subfamilies of the Exocoetidae. Evidence at barbel variability in size and/or number has been used by various workers to assess the value of barbels in terms of homology and phylogeny. For example, in the cyprinid Hybopsis, subgenus Erimystax, barbels of H. harperi generally are minute or lacking on one or both sides: in other species of Hybopsis, barbels are usually well developed (Hubbs & Crowe, 1956). In H. aestivales, some specimens have two pairs while others have only one pair of barbels (Yerger & Suttkus, 1962). In H. lineapunctata, there is a single pair of maxillary barbels but several specimens lack them (Clemmers & Suttkus, 1971). Indeed, the existence of specimens of Hybopsis and Notropis with or without barbels, invalidates this structure as a generic or specic character (Cortes, 1968). Likewise, 87% of Notropis emiliae lacked a barbel, 11% had a single small one and about 1% (2 of 159 specimens) had a pair of barbels. Only nuptial males of Pimelodes notatus possess them (Gilbert & Bailey, 1972). Schmidt (1983) also reported variation in the size and presence of barbels in the cyprinid Rhinichthys cataractae. Among 126 specimens 3.812.6 cm SL, 6 had no barbels and 14 lacked a barbel on one side or the other. Gilbert & Bailey (1972) argued that the absence of barbels in ancestral characoid shes and their diversity in location, structure and number around the mouth in numerous cyprinids, point to their repeated independent development and loss. They grouped the N. American cyprinids into six structural groups, indicating many evolutionary lines. Schmidt (1983) likewise did not recommend barbels as a character for generic classication in N. American minnows. He believed that barbels should be treated with caution in classifying species; that barbels were either apomorphic (derived from pre-existing structures) or plesiomorphic (primtive) structures. He preferred, albeit lacking evidence, apomorphy, a view which would appear to be supported by work of Collette (1984) on Exocoetus (vide supra). Other workers attached no phylogenetic signicance to the presence or absence of barbels, for example Fahay & Markie (1984) in Gadiformes and Fink & Fink (1981) in ostariophysans. Many cypriniforms and all siluroids have maxillary barbels situated at the rictus of the mouth, sometimes associated with the tip of the maxilla. In siluroids, the barbel extends from the distal part of the maxilla, and the skin of the maxilla and barbel is separated from cheek skin by a deep cleft.

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Figure 5. Ultimostomias mirabilis a deep-sea stomiatoid sh with an elongate barbel 417 mm long (sh 43.7 mm long). (A) lateral view (X 2.4); (B) short length of barbel enlarged. Half the barbel, probably the anterior part, has dark spots; the other half has a series of white light organs alternating with what is claimed to be a small photophore (From W. Beebe 1933, Copeia No. 4).

Other ostariophysans and primitive teleosts have no barbels. There is well documented information on the evolutionary lability of barbels of cypriniforms and siluroids. The presence of posterior maxillary barbels is the only barbel feature common to the primitive members of both groups. All the other barbels (submental, nasal, anterior maxillary) occur in various combinations in advanced cypriniforms and siluroids. This lability of barbels, together with the extensive number of characters that mitigate against an hypothesis of a close relationship between cypriniforms and siluroids, plus the fact that barbels are lacking in characiforms and gymnotoids, led Fink & Fink (1981) to conclude that barbels evolved independently, perhaps several times, in the two lineages. This view is in agreement with that of Gilbert & Bailey (1972) for the Cyprinidae. In further support, Howes (1991) showed that among bariliine cypriniforms some specimens have anterior and posterior maxillary barbels, some only posterior ones and others have no barbels. Other cypriniforms show similar barbel distribution and in-

traspecic variability is not uncommon. Howes (1991) also believed that the origin of barbels, within the cypriniforms, has been of frequent occurrence. Nevertheless, cyprinids develop barbels during the last third of the larval period, often when they are juveniles after n-fold absorption and siluroids and cobitoids develop them during the rst third of the larval period, sometimas before hatching: barbels of cobitoids appear to originate slightly later in development than those of sliuroids. Such differences heterochrony in barbel origin and development in the three groups, might well have some importance in classication, at least in the case of the siluroids (Fuiman, 1984). It would seem, therefore, that from the substantial morphological evidence available (including the limited information on ontogeny), caution should be exercised when comparing barbeled and non-barbeled forms within and between families and species. Barbels my be present, or never have arisen, or show secondary loss or fusion, features best determined by an investigation of their ontogeny. Evidence of phylogenetic relationships between and within families, on

162 the basis of barbel presence, structure, number, location or primitiveness as judged by their absence, might well be of value but only within the framework of a multitude of other morphological characters, that should be compared and contrasted. The general consensus is that barbels have originated independently a number of times in different groups of shes. They may be derived or apomorphic in some cases, or in others may be primitive, originating sui generis. Presumably barbels are homologous within families. Possibly they have some use in classication, at least in siluroids with numerous barbeled families, though barbels are of little value in determining sh phylogeny. Finally, the question my be posed why did barbels arise in shes? Presumably, it is likely that an increased exploitation of food reserves at the littoral bottom led to a demand for a simple chemosensory (and tactile) system on the lips and jaws of shes, vision being less effective for inspection of food in dark habitats. Evolutionary development would include modication of the pharyngeal jaw apparatus and musculature, and in some cases the origin and differentiation of barbels, with a high degree of gustatory and tactile sensibility in seeking food (see Sibbing, 1991). Fish with barbels feed on zoobenthos, seen for example in Eurasian cyprinids that also have thick rubbery lips; they are usually concerned with sucking food from and around stones (Baranescu & Coad, 1991). Such anatomical modications, doubtless originated any time during the phylogenetic history of shes. bels with a central cartilaginous or osseous) rod-like skeleton, extending from the base along its length. Indeed Zincone (1876) long ago described a cartilaginous skeleton in those of Ictalurus and a bony one in Lota and Mullus barbatus. The skeletal rod of the barbels of Pimelodus clarias and Ictalurus nebulosus was believed by Ghiot & Bouchez (1980) to be composed of elastin. However, in a wide ranging examination on cranial cartilage of teleosts, Benjamin (1990) showed that elastic/cell rich cartilage is typical of barbels and the maxillary oral valves. In Corydoras melae this cartilage type is present in the bid mandibular and in the maxillary barbels, where in the latter the cartilage ts into a hollow in the maxilla, as in Pimelodes clarias (Ghiot & Bouchez, 1980). In Leiocassis siamensis, Clarias batrachus and Pimelodes pictus, the cartilage is in continuity with a root piece (see Pollard, 1894), to which is attached the protractor hyodeian musculature (Benjamin, 1990). In cyprinids and silurids, an independent cartilage occurs on either side above the nasal organ (called a Nasenugelknorpel or a nasal alar cartilage by earlier workers). In the silurids, in particular, this cartilage supports the nasal barbel (Norman, 1926). Baeker (1926) appears to be the rst to classify barbels as 1. tender and yielding, without a cartilaginous or bony skeleton: 2. barbels rigid (with bone) and exible (with cartilage). Sato (1937d) subsequently grouped Japanese sh barbels (18 species of 11 families) into Barbel histology Among various Japanese, Indian and European freshwater and marine shes, Sato (1937ad, 1938, 1977a, b) and Sato & Kapoor (1957) described the barbels by light microscopy. The elongated cylindrical barbel is covered by a multilayered epidermis with pear-shaped taste buds (vide infra), though these may be absent, for example, in barbels of Pristiophorus japonicus (Sato, 1937d) and Mystus vittatus (Agarwal & Rajbanshi, 1965). Mucous and club cells (and also Merkel cells, see Whitear, 1989), also occur in the epidermis. The dermis and more central regions contain layers of collagenous connective tissue, blood vessels, chromatophores, myelinated nerves (branches of the trigeminal and facial) and muscles (Sato, 1937ad; Sato & Kapoor, 1957). Many species of sh have bar1. barbels without taste buds: 2A those with taste buds in the epidermis and without cartilage (Cyprinidae, carps); 2B barbels with taste buds and cartilage (catshes, goatshes, loaches); 2C barbels with an axial rod of striated muscle (Polymixia type). Barbels of the carp and catsh are of the tender and exible type respectively (Sato & Kapoor, 1957), those of Arias thalassinus are of the exible type (Kapoor & Bhargava, 1967). Among teleosts, barbels of Gaidropsarus, Gadus and Lota (and also Acipenser) have cartilage (Meng, 1923). A Knochenkorper or a Knorpelkorper in those of Gadus, Silurus and Acipenser sturio were described by Baeker (1926). An osseous skeleton was

163 reported in barbels of Gadus microcephalus (Sato & Kapoor, 1957). Members of the Mullidae, Siluridae, Cobitidae and Pristiophoridae likewise have barbels with cartilage (Sato, 1937d), as well as in those of Clarias batrachus (Srivastava & Singh, 1961), Bagarius bayad (von Lucwicz, 1966) and B. bagarius (Nagar & Mathur, 1958), Arias thalassinus (Kapoor & Bhargava, 1967), Rita rita (Singh & Kapoor, 1967) and Mullus surmuletus (Ono, 1979). Barbels of the channel catsh Ictalurus punctatus have a skeleton of cartilagelike substance (Grizzle & Rogers, 1976), though true cartilage occurs in barbels of Ictalurus nebulosus (Rafn-Peyloz, 1955). All 11 barbels on the head and lower jaws of Blepsias cirrhosus draciscus (Cottidae) have cartilage (Sato, 1977a) (see Figures 4, 6A, B). The fringed blenny, Azuma emnion and Hemipterus villosus have similar cutaneous barbel-like processs, albeit lacking a supporting axial skeleton and blood vessels. They do have epidermal terminal buds; presumably they act as feelers to recognize food (Sato, 1977b). Among the barbels of Misgurnus fossilis (Cobitidae), only the labial externus has a cartilaginous skeleton (Ducros, 195354). In contrast, a number of shes have barbels without skeletal support, the centre occupied by connective tissue, nerves, blood vessels and muscle. These include Cyprinus (Baeker, 1926), conrmed in the Cyprinidae (Sato, 1937d; Srivastava & Singh, 196l), Labeo calabasu (Cyprinidae) and Noemacheilus corica (Cobitidae) (Nagar & Mathur, 1958) Barbus bynni (von Leucowicz, 1966) and Agonus cataphractus, which has extensive elastic tissue associated with central collagen (Whitear & Mittal, 1986). Meng (1923) described circular and longitudinal muscles in barbels of Cyprinus carpio, Gadus aeglenus and Acipenser sturio. Muscles in barbels of Gadis were also reported by Baeker (1926). The central region of the barbel, nevertheless, is most diverse in content and Rafn-Peyloz (1955) believed that Meng (1923) confused muscle with collagen and nerve bundles. The presence of an intrinsic and extrinsic musculature associated with the barbels would appear to be variable (vide infra). Thus barbels of Mullus surmuletus have a skeleton but no intrinsic muscles and those Polymixia lowei are without a skeleton along its length but have an intrinsic musculature (Ono, 1979, 1982). Taste buds of barbels There is a variety of different cell types in barbel skin (Whitear, 1986, 1989 and vide infra. Indeed, Joyce & Chapman (1978) described at least 10 types, though probably some are different developmental stages of the same cells. However, the most signicant organs in barbels are the taste buds and these have received the most attention. Brief history and distribution Taste buds, rst described by Weber (1827) in the palatal organ of the carp and later by Leydig (1851) in various teleosts, are especially rich in barbels. Schulze (1863, 1870) described the Becherformigen Organe of Leydig in skin of Tinca chrysalis and barbels of Barbus vittalis and later on in skin of other shes. He distinguished sensory from supporting cells in the organ and contrasted them with neuromast cells of the lateral-line, believed by Leydig to be the same type of cells. Jobert (1872) also found taste buds (he believed them to be tactile) in shes. Sense organs of the pouting and rocklings, in similar skin areas described by Wright (1884), were believed by Bateson (1890) to resemble taste buds of higher forms. They also occur in the lips and barbels of Acipenser ruthenus (Dogiel, 1897; see also recent work by Pevzner, 1981a, b, 1985; and a brief historical review of taste buds in vertebrates by Reutter & Witt, 1993). Taste bud-like formations are present in the epidermis of the orbital cirrhi (shaped like a hand), of Hypsoblennius gilberti among the Perciformes (von Bartheld & Meyer, 1985). Among elasmobranchs, taste buds only occur in the mouth (Cook & Neal, 1921); in the tongue palate and pharynx of Squalus africanus and Heterodontus (Kapoor et al., 1975) and Trygon pastinaca and Raija clavata (Pevzner, 1976) and oral papillae and oral valves of Scyliorhinus canicula (Moate & Whitear, 1994). Among cyclostomes, the sensory end buds of the tentacles of Myxine glutinosa and Eptatretus burgeri were considered to be similar in structure and function to those of bony shes (Patzner et al., 1977); Georgieva et al., 1979) (see Figures 7, 8). Ultrastructure There is an extensive literature on the barbel taste buds of shes, especially since Trujillo-Cenoz (1961) described their ne structure (see also reviews among

164

Figure 6. Micrographs of transverse sections of the barbel of Blepsias cirrhosus draciscus. (A) anterior snout barbel, ar axial cartilaginous rod; bv blood vessel; d dermis; ecc elongated cylindrical cell: m melanophore; n nerve bre, tb terminal bud. (X 60). (B) Supraorbital barbel. gc granular cell. (X 1200). (Figures 4 and 6 Courtesy of K. Sato 1977, Jap. J. Ichthyol. 23).

others by Kolmer, 1927: Bhatti, 1952; Cordier, 1964; Hirata, 1966; Graziedei,1969; Schulte & Holl, 1971; Breipohl et al., 1974; Kapoor et al., 1975; Reutter, 1978, 1982, 1987; Vinnikov & Pevzner, 1981; Tucker, 1983; Kinnamon, 1987; Caprio, 1988; Jakubowski & Whitear, 1990). Doubtless because of their accessibility, there are numerous descriptions, using transmission electron microscopy (TEM), of taste buds in barbels, for example in Ictalurus punctatus (Grover-Johnson &Farbman, 1976; Joyce & Chapman, 1978); I. nebulous (Reutter, 1978); I. melas (Desgranges, 1965, 1966, 1972); Corydoras paleatus (Trujillo-Cenoz, 1961; Cordier, 1964; Schulte & Holl, 1971; Fujimoto & Yamamoto, 1980); Cyprinus carpio (Uga & Hama, 1967); Ciliata mustela (Crisp et al., 1975); Cyp-

rinus, Misgurnus and Parasilurus (Toyoshima et al., 1984); Cyprinus carpio, Parasilurus asotus and Cobitis biurae (Hirata,1966; Changolin & Zuohua, 1981); Clarias, Kryptopterus and other teleosts (Welsch & Storch, 1969; Storch & Welsch, 1970) and Silurus glanis and Plotosus lineatus (Reutter & Witt, 1993). Scanning electron microscopy (SEM) was used by Ovalle & Shinn (1977) to describe taste buds of catsh barbels (Figures 13), Jakubowski (1983) used TEM and SEM for taste buds, including those in barbels of the spined loach, Cobitis taenia and Jakubowski & Whitear (1990) likewise described oral and external taste buds, including in some cases those of barbels, in an extensive series of teleosts (see also Whitear, 1971; Lane & Whitear, 1982).

165

Figure 7. Diagrammatic representation of a taste (sensory) bud in the tentacle of Myxine glutinosa. B basal cell; BM basement membrane of the epidermis; N nerve bre; NP branch of nerve plexus; R receptor cell; Sg glandular supporting cell type III; St supporting cell type II; SZ mucous cell. Courtesy of V. Georgieva et al., 1979, Zool. Scripta 8).

Figure 8. Diagrammatic representation of a taste bud of Ictalurus. Synaptic contacts occur basally on the light (Sl) and dark sensory cells (Sd). B basal cell; Bl basal lamina; BV blood vessel; M marginal cell; NF nerve bre; NM mylelinated taste bud nerve. (Courtesy of K. Reutter 1986, Biology of the Integument 2: Vertebrates, Springer, Heidelberg).

In general, in shes, from all regions of the body, either internally or externally, taste buds, apart from size and number per unit area, show a common uniform structural arrangement of their cellular components (see Kotrschal et al., 1991). For example, oral taste buds of Sprattus sprattus (Jakubowski & Whitear, 1990) possess all the structural features, in miniature, described by Hirata (1966) in the barbels of other shes. The pear-shaped taste bud extends almost right across the stratied epidermis, usually its base situated on a small dermal papilla, albeit missing in rockling barbel taste buds (Zincone, 1876; Bateson, 1890). Apical cell processs of the taste bud, at the free surface of the skin (receptor eld), usually occupy a pore of variable size in different species.

Taste bud sensory cells vary in number within and between different species, ranging from ve in Pomatoschistus and 67 in Corydoras (Jakubowski & Whitear, 1990), to 100150 in taste buds of barbels and n rays of Ciliata mustela, where about twothree of them are sensory cells. Crisp et al., (1975) also calculated that in the underlying nerve plexus, there are nerve bundles, each of about 35 axons, a total of about 230 axons per bud. A capillary loop vascularises the taste bud. According to Desgranges (1965, 1966), there are ve types of sensory cells in barbels of Ictalurus melas, a view based mainly on differences in size and shape. However, these sensory cells are probably different forms of similar cells. The terms t (tubule) for gustatory cells and f (brillar) for the supporting cells, were used by Crisp et al., (1975). Furthermore, among others, Welsch & Storch (1969), Storch & Welsch (1970), Grover-Johnson & Farbman (1976), Joyce & Chapman (1978) and Reut-

166 ter (1978, 1986) considered that the elongated sensory cells of the barbel taste buds were light EM-lucent cells (with sER and microtubules etc., that terminate apically in a single broad microvillus), and dark EM-dense cells with a dark cytoplasm, more granular inclusions, tonolaments, sER and rER and an apex of several microvilli). They interpreted the supporting cells (see Trujillo-Cenoz, 1961) as dark sensory cells (but vide infra). Proximal lobated processes of both cell types appear to interdigitate with nerve bres (Figure 7). Comparable body taste bud sensory cells, of Raia and Trygon, have 312 apical microvilli (Pevzner, 1976). Below the sensory and supporting cells usually there are up to ve basal cells, oriented transversely, though they are not found in taste buds of the n and barbels of rocklings Caidropsarus and Ciliata (Crisp et al., 1975; Whitear & Kotrschal, 1988), or in the external taste buds of Anguilla, Lota, Poecilia and Colisia (Jakubowski & Whitear, 1990). There are no taste buds in barbels of the silurid Mystus vittatus and those in the body are without basal cells (Agarwal & Rajbanshi, 1965). The view that light and dark cells of the taste buds are distinct sensory cells was denied by Jakubowski & Whitear (1990) who concluded, in this case, that the EM-density reects cell age and that an extreme EMdense cytoplasm is a feature of cellular degeneration, or of mechanical damage. They advocated the abandonment of the light-dark nomenclature. Furthermore, they considered that direct synapses between different cells of the taste bud (light, dark and basal cells) (Reutter, 1986: Reutter & Witt, 1993), have not yet been established with any degree of certainty. Other membrane cisternae may occur near nerves, but the evidence so far is not conclusive that they are synaptic. However, some at least of the taste bud component cells are innervated. For example, in the taste buds of the oropharyngeal cavity and head skin of Tinca tinca, Zuwala & Jakubowski (1993) described synaptic associations, from the afferent nerve plexuses, on the basal and gustatory (sensory) cells but not the supporting cells. Presumably, therefore, there is nervous regulation of taste bud activity. Recently Finger & Bottger (1990) used a carbocyanine dye (1,1 diocadecyl-3,3,3, 3-tetramethylindocarbocyanine perchlorate) (dil), applied to the nerve stumps of isolated barbels of Ictalurus punctatus. Ultimately (seen by epiuorescence), some labeled axons innervated the taste buds or ended freely in the epidermis. A limited number (veten) of the receptor cells in the taste bud was labeled by transcellular passage of dye from the nerve endings. Occasionally labeled taste bud basal cells were seen. Such labeling may well demonstrate a relationship between specic receptor cells of the taste buds and their innervation, presumably related to their functional mechanisms. Some measurements of barbel taste buds Taste buds are particularly numerous in the body and barbels of shes in silty waters, presumably to compensate for poor vision (Moore, 1950). Barbels usually have their taste buds most heavily concentrated at the tip, though the numbers in different species appear to be variable. For example, in barbel skin of Cobitis taenia, per sq.mm Jakubowski (1983) reported 90160 taste buds, with more in the mouth and up to 370 near the oesophagus. In Ictalurus nebulosus, per sq. cm of barbel skin, there are 1675 with 3400 at the tip (Bardach et al., 1969). In Ictalurus natalis Atema (1971) reported 20 000 taste buds in the 8 barbels; there are also 3000 (lips); 155 000 (body); 8000 (mouth) and 12 500 (gill arches), a total of about 200 000 taste buds in the entire sh. High numbers of taste buds in barbel skin of Ciliata mustela, up to 14 000 per sq. cm near the tip, were reported by Crisp et al., (1975). Taste buds generally vary in size in barbels of different species of teleosts (see Table 2). To some extent size correlates with epidermal thickness, for in barbels of Cillata mustela, at the tip the epidermis is 5060 m thick and the taste buds are 3045 m high: at the base the epidermis is 75 m thick and the taste buds are 3055 m (Crisp et el., 1975). Barbel taste buds of Corydoras, 3050 m high, each have 4080 receptor cells and a comparable number of supporting cells (Fujimot & Yamamoto, 1980). There are 35 basal cells, similar to those described by Hirata (1966), a number typical for most teleost taste buds (Reutter, 1986, Reutter & Witt, 1993). Taste buds of barbels of Ictalurus punctatus, 5080 m high and slightly less in width, have about about 60110 each of the so-called light and dark sensory cells, all about 50 60 m high and 1015 m wide. There are threeve basal cells in the taste buds of this species, with many unmyelinated nerves between them (Grover-Johnson & Farbman, 1976). The sensory buds in the tentacles of Myxine glutinosa, containing receptor (Type I) and supporting (Types 11 and 111) cells, are similar in appearance

167
Table 2. Measurements of taste buds in barbels of some teleosts. Those by Sato (1937a, 1938) are of chin barbels; those of Bath (1962) are of Maxillary barbels Height Upeneus spilosus Upenoideus bensasi Parasilurus Pelteobagrus Pseudobagrus Leobagrus Peristedion amiscus 30 Peristedion orientale Cyprinus Parasilurus Cobitis Ciliata mustela Ictalurus Lota Corydoras Tinca Hemidactylus 20 (Sato, 1937d) 4575 3050 30-55 5390 5988 5073 4473 4470 5075 3859 2950 2032 2333 2029 (Hirata, 1966) (Crisp et al., 1974) 110 120 Width (m) 70 80 (Sato, 1938) (Sato, 1937a)

80

40

Monoamine uorescence is recognized in basal cells of barbel taste buds of Cyprinus carpio and Parasilurus asotus (Hirata, 1966; Nada & Hirata, 1977). In Misgurnus, Parasilurus and Cyprinus, such cells in their barbels display an intense yellow uorescence (Toyoshima et al., 1984). The taste buds of Ictalurus are reported to be innervated cholinergically and aminergically (Reutter, 1978), For further information on taste bud histochemistry see Kapoor et al. (1975) and Reutter (1986).

Other specialized cells in barbel skin The mucous (goblet) cell is an exocrine unicellular gland, whose intact membrane-bounded globules discharge their contents at the skin surface. They were described, for example, in barbel epidermis of Cyprinus, Motella, Lota and Acipenser (Meng, 1923) and in barbels of cyprinids and silurids (which also include club cells) (see Sato, 1937d; Rafn-Peyloz, 1955; von Lucowicz, 1966). Mucous cells are numerous in barbels of Misgurnus but are fewer in those of Cobitis (Ducros, 195354). Club cells, another category of mid-epidermal secretory cells, of characteristic ultrastructure (Whitear, 1986), are the Schreckstoffzellen, which in the Ostariophysi at least, secrete the pheromone of the fright reaction (Pfeiffer, 1977). There is considerable variability in the distribution of mucous and club cells in the barbels of different species of teleosts (Sato, 1937d; Sato & Kapoor, 1957. They are missing in barbels of Bagarius bagarius (Nagar & Mathur, 1958) and in those of Haplogenys nigripennis; only few mucous cells occur in the barbels of Aptistus evolans and Noemacheilus corica (Sato, 1937d). Mucous cells are smaller and more numerous than the club cells in barbels of Heteropneustes fossilis and they are absent in those of Podothecus and Gadus macrocephalus (Sato & Kapoor, 1957). Likewise, club cells are scarce in barbels of Arius thalassinus (Kapoor & Bhargava, 1967): they were not found in those of Wallago attu and Clarias batrachus (Rajbanshi, 1975) and in Ictalurus punctatus (Grizzle & Rogers, 1976), though Joyce & Chapman (1978) later described club cells in barbels of this species. There is evidence of variation in the distribution of mucous and club cells within the barbel. Mucous cells occur in those of Rita rita but here club cells are missing in the distal region (Singh & Kapoor, 1961).

(Bath, 1962)

to those of teleosts. They have an apical diameter of 28 m and are about 48 m high 60 m wide (Georgieva et al., 1979). Histochemistry In barbels of Saccobranchus fossilis, the nuclei of the gustatory and supporting cells of the taste buds contain alkaline and acid phosphatase, possibly concerned with nucleic acid synthesis (Rajbanshi & Tewari, 1968). ATP-ase and 5-nucleotidase are present in the epithelium of head and barbel skin, including the constituent cells of the taste buds, though the gustatory cell processes are negative to both enzymes. Non-specic esterase occurs in both cell types (including their cell processes) of the taste buds (Tewari & Rajbanshi, 1971). The basal cells of the taste buds of barbels of Ictalurus contain glycogen (Desgranges, 1972). Succinic dehydrogenase, lactic dehydrogenase and glucose-6-phosphatase occur in all barbel tissues: 5hydroxy-tryptomine is present in the taste buds and monoamine-oxidase exhibits high activity in the basal cells (Reutter, 1971, 1987).

168 In Noemacheilus corica, among the few mucous cells, they are missing apically in the barbel: club cells are scarce in the proximal region (Nagar & Mathur, 1958). Merkel cells occur in the epidermis, at various levels, in at least 12 species of teleosts (and lampreys too); they are about 46 m in diameter (see Whitear, 1989). These cells occur in barbel epidermis of Ictalurus melas (Lane, 1977; Lane & Whitear, 1977), Cyprinus carpio (Tachibana et al., 1984), Gaidropsarus and Ciliata (Whitear, 1989). Merkel cells are sparsely distributed among the barbel taste buds in different layers of epidermal cells of Cyprinus. They are about 7.5 m in diameter, somewhat larger than those in body skin of other teleosts, with cell processes and dense-cored granules 75100 nm wide: nerve bres contact the cells. Tachibana et al. (1984) believed that the Merkel cells have a secretory function. However, it is reasonable to assume that Merkel cells in sh barbels are, like those of amphibians, associated with synaptic nerve bres that are mechanoreceptive (Parducz et al., 1977); that the main function of the Merkel cell-nerve unit in barbels is for mechanoreception, as in skin of other vertebrates. This would support the view that barbels have a tactile function, in addition to chemosensibility (vide infra). The epidermis of barbels of Agonus cataphractus contains numerous chloride cells (ionocytes) but only few sacciform cells and goblet cells are missing as in the rest of the skin (Whitear & Mittal, 1986). Presumably the chloride cells mediate ionic exchange, as do similar cells in the body of euryhaline shes. During the ontogeny of barbels some may ultimately disappear. Thus among four species of Indian catshes, Karamchandani & Motwani (1956) described the early appearance of barbels in larvae of Silonia silondia (6.7 mm), Ailia coila (6.8 mm), Ailiichthys punctatus (6.7 mm) and Gagata cenia (4.2 mm). Four pairs of barbels (nasals, anterior and posterior mandibular and maxillary) are retained through development and adulthood in Ailia and Ailiichthys and three pairs are well developed in Gagata. However, in Silonia silondia (6.7 mm long) with three pairs of barbels, the nasals are the shortest (1 1/2 diameter of the eye), the largest maxillary barbels reach the vent and the mandibular barbels reach the gill openings. In a 10.8 mm larva the barbels have shortened somewhat and considerably so in the 14.3 mm larva: nasals 3/4 diameter of the eye), maxillary barbels reach the gill openings and the mandibular barbels just reach the eyes. Only minute maxillary barbels persist in the adult Silonia silondia. The nasals rst disappear in the 12 14 mm sh, then the mandibular barbels in the 1517 mm sh. Silonia childreni retains two pairs of barbels in adults (Karamchandani & Motwani, 1956). The development and life history of Rita rita, including that of its barbels (see Karamhandani & Motwani, 1955), are generally similar to the other catshes previously described with the exception of Silonia silondia. In larvae of Rita rita at stage IV (24 h old, 5.8 mm long), rudimentary barbels rst appear; they are clearly seen in stage V (36 h). By stage VI (44 h,6 mm long) maxillary barbels and mandibular barbels are well developed and by stage VIII (3 1/2 days, 8 mm long), though yolk is not completely absorbed, three pairs of barbels are present. The larva now has two rows of teeth on the jaws and the nfold is broad and continuous. At 6 1/2 days the post-larval stage 11 resembles the adult with three pairs of retained barbels. During larval development in some forms barbels may fuse together into a single structure, often to become fringe-like, as in exocoetids (Collette et al., 1984). Barbels are single in Exocoetus monocirrhus and species of Cypselurus, or paired in Parexocoetus brachypterus and all species of Cheilopogon (see Kovalevskaya, 1982). Atoda (1935) described in some detail the development of the barbels in Parasilurus asotus (Figures 9ad). At hatching larvae are about 4 mm long: Anlagen of the pectoral ns are slightly pigmented and myomeres discernible. Anlagen of the larger paired

Early development of barbels: maintenance: regeneration Barbel origin Cyprinids develop barbels late in larval life or in juveniles. Barbels originate in siluroids early in larval life, sometimes before hatching and in cobitoids a little later (Fuiman, 1984). Mental barbels of gadiforms usually appear during the early larval period or in early pelagic juveniles (Fahay & Markle, 1984) and in exocoetids, among the Beloniformes chin barbels, likewise develop in juveniles (Kovalevskaya, 1982; Collette et al., 1984). Among melanostomiatids of the Stomiiformes, barbels develop in postexion larvae, for example in Bathophilus brevis (Kawaguchi & Moser, 1984).

169

Figure 9. Larvae of Parasilurus asotus showing the development of the barbels. (a) Larva just hatched; body length 4 mm. (A) ventral and (B) side views. (b) Larva 43 h after hatching; body length 5.8 mm. (A) side and (B) ventral views. (c) Larva 8 days after hatching; body length 8.4 mm. (d) Older larvae 2 cm and 5.1 cm long. a anal n; aa analage of anal n; ac anlage of caudal n; ad analage of dorsal n; aml anlage of rst permanent mental barbel; am2 anlage of second temporary mental barbel; ap anteror anlage of pectoral n; c caudal n; d dorsal n; h heart; m mouth; mb maxillary barbel; ml rst mental barbel; m2 second mental barbel; p pectoral n; v ventral n; y yolk. (From K. Atoda 1935, Sci. Rept. Tohoku Imp. Univ. Ser. Biol. Vol. X).

170 maxillary barbels, at the outer edge of the mouth and of the mental barbels, appear as wen-like processes. Anlagen of the second pair of mental barbels are also present. Two days after hatching (larva 5.8 mm long), Anlagen of the anal and caudal ns are recognizable. The maxillary barbels are well developed but the two pairs of mental barbels are less prominent. After 8 days post-hatching (larva 8.4 mm long), the dorsal n has appeared. All the barbels are well developed, the second pair of mental barbels (missing in the adult) slightly longer than the rst pair. However, in the larva 34.5 cm long, the two pairs of mental barbels are of similar length and when the larva is 67 cm long, the second pair drop off and disappear (Atoda, 1935). In Ictalurus, taste buds, that are prominent barbel components rst appear in the ectoderm of the anterior oral cavity and on the rst three gill arches: ultimately they spread to the lips and thenceforth over the body (Landacre, 1907). It seems likely, therefore, that the taste buds on the body and barbels are ectodermal in origin, and those present in the oro-pharyngeal cavity are either endodermal (Cook & Neal,1921; Edwards, 1930, or possibly from both sources (see Kapoor et al., 1975). Evidence obtained from experiments on taste bud regeneration showed that the basal lamina, initially located above the glial Schwann cells, disappears and below them a new lamina forms. Reutter (1982, 1986) concluded that the glial cells became the basal cells of the taste bud, of neurectodermal origin, in contrast to the ectodermal origin of the sensory and supporting cells. Maintenance and regeneration of taste buds That barbels can regenerate has been well documented, for after amputation catsh barbels regenerate nerves, cartilage, connective tissue, epidermis and taste buds, all dependent upon the regenerated nerves (Kamrin & Singer, 1953, 1955). Recent work has described the small chin barbel of Lota lota to regenerate several mm in length within 3 months, after transection at the base (Cochran, 1987). Whitear (1990) showed that, in Heteropneustes fossilis, after amputation of the barbel, within two days post-operation the stump was covered by epidermis and by the third day regeneration tissue was present. There was 1 1.5 mm of regenerated tissue (5 days) and 2.43.5 mm (78 days), about 0.5 mm growth per day. The axis contained blood vessels, regenerated nerves with Schwann cells, broblasts and collagen but no cartilaginous skeleton. Tissue remodeling included simultaneous phagocytosis and synthesis of collagen by broblasts. The absence of cartilage in the regenerated barbel may well be due to a deciency of chondroblasts from the perichondrium, for Raghuvanshi (1980) earlier showed that in H. fossilis, by selective removal of cartilage in various regions of the barbel, successful regeneration of cartilage required sufcient aggregation of chondroblasts to promote chondriction. Earlier classical experiments by Olmstead (1920a, b) on the catsh barbels clearly demonstrated that, after section of the facial nerve supply, the taste buds degenerate and are phagocytosed by leucocytes. They reappear on the restoration of the nerves, the cycle taking about 40 days. Olmstead believed that a nerve hormonal factor(s) transformed epithelial cells into taste bud cells and inuenced their maintenance and functional state. May (1925) showed, among other things, that after nerve section, taste bud regeneration begins only when the regenerated barbel nerve reaches the area of the degenerate taste buds: again a nerve substance was considered to inuence taste bud growth and integrity. These results were conrmed by Olivo (1928) and by Torrey (1934, 1936), who showed that low temperature inhibits nerve regeneration and hence the reappearance of the taste buds, the most efcient temperature being 20 . The causative inuence might be enzymatic in character. The dependence of barbel taste buds on their nerve supply was later conrmed by Wagner (1953) and Guth (1971). According to Geraudie & Singer (1977), denervation of the mandibular barbels of Ictalurus nebulosus resulted in a proximo-distal degeneration of the taste buds, beginning on day two, to completely degenerate and disappear by day 9 (22 C). Taste buds start to reappear in the barbel epidermis by day 16, as the nerve regenerates and re-innervates them. In contrast, Desgranges (1978) found that, after nerve transection, the taste buds of the mental barbels of Ictalurus melas remain apparently normal in appearance for up to three weeks (20 C), before they disappear (see also Wagner, 1953). The sustentacular cells persisted for a longer time than the sensory cells, Differences in taste bud survival time, during degeneration, were believed by Desgranges (1978) to relate to the greater length of the nerve bres supplying the taste buds. However,

171 their dependence on a functional nerve supply is not disputed. Within the taste buds of barbels of Ciliata mustela, there is a small number of degenerate cells, a feature of their rapid turnover and replacement, considered to be from peripheral cells (Crisp et al., 1975; see also taste buds in the dog and rat tongue, Olmstead, 1921; Beidler & Smallman, 1965). Whether individual cells in the taste bud normally divide is not clear. Jakubowski & Whitear (1990) found one mitotic cell high up in a taste bud of Ictalurus, but this feature may have been a rare event. The average life span of the catsh barbel taste bud cells is temperature-dependent: 40 days (l4 C); 30 (18 C); 15 (22 C); and 12 (30 C) (RadermanLittle, 1979). However, it is possible that gustatory and supporting cells may be renewed at different rates (Kitoh et al., 1981). The time taken for taste bud renewal in Ictalurus punctatus (at 30 C) and rats and mice (at 37 C), is similar, 1012 days (Caprio, 1988). Among previous workers on barbel histology, some described centrally situated muscle within the barbel (Meng, 1923; Sato, 1937a, d; Ducros, 195354; Sato & Kapoor, 1957); others did not mention it (Nagar & Mathur, 1958; Srivastava & Singh, 1961; Agarwal & Rajbanshi, 1965; von Lucowicz, 1966; Rajbanshi, 1966; Hirata, 1966; Kapoor & Bhargava, 1967; Rajbanshi & Tewari, 1968). Muscle was reported in barbels of some species but not in others (Sato, 1931d; Sato & Kapoor, 1957). Nevertheless, in some cases at least collagen may have been mistaken as muscle (see Rafn-Peyloz, 1955). However, Ono (1979,1982) demonstrated, by electron microscopy, intrinsic striated muscle in barbels of Polymixia lowei, which have no elongate axial skeleton and their absence in barbels of Mullus surmuletus, which have one. Some barbels, for example those of Blepsias cirrhosus, which have no muscle, appear to move passively by water currents (Sato, 1937a). Other barbels are claimed to move voluntarily, for example those of Upenoides bensasi (Sato, 1937a) and some catshes (Singh, 1967), presumably by the use of extrinsic muscles (vide infra). Likewise, movement of some barbels with a skeleton, of Callichrous, Heteropneustes and Podothecus, is effected by extrinsic muscles situated basally (Sato & Kapoor, 1957; Benjamin, 1990). The presence or absence of a skeleton in the barbel could well be related to its range of movement, for in Ictalurus nebulosus, basally the cartilage joins the head by a joint that permits a limb-like movement (Biedenbach, 1971). Barbels without a skeleton, of Barbus sarana and Botia loharchala, become turgid and erectile and have a hydrostatic skeleton, by the expansion of blood vessels at the centre (Sato & Kapoor, 1957). Alexander (1965, 1966) described three different mechanisms for catsh barbel movement, effected by abductor tentaculi and adductor mandibuli muscles. Movement of the maxilla swings the barbel downwards to locate food. Extrinsic muscles inserted on the quadrate, maxilla and palatine likewise elicit barbel movement in some cyprinid and silurid shes (von Lucowicz, 1966). Maxillary barbels of silurids are moved by retractor tentaculi (innervated by branches of the r.maxillo-mandibularis V and r.mandibularis V) and extensor tentaculi (innervated by a palatine branch of the r.hyomandibularis VII), inserted on the maxilla and palatine bones. The mandibular barbels are moved

Barbel movement Pollard (1894) described the four barbels of Myxine to contain procartilage that continued into a rootpiece, a hard yellow spongy, intercellular matrix tissue, with which intertentacular muscles are associated, supplied by branches of the trigeminal nerve. In siluroids, the premaxillary, maxillary and coronoid barbels, of the upper jaw and the mental and submandibular barbels of the lower jaw, likewise contain a rootpiece associated with muscles (except for the coronoid) and innervated by the trigeminal nerve. In the teleosts Pimelodus pictus and P. clarias, the proximal end of the rootpiece of the maxillary barbel is inserted into a hollow region of the maxilla (Ghiot & Bouchez, 1980; Benjamin, 1990). The rootpiece in the barbels of Silurus glanis anchors the barbel to the geniohyoid (protractor hyoid) muscle (Hoffman, 1923). Likewise, in Leiocassis siamensis and Pimelodus pictus the rootpiece anchors the external protractor hyoidei muscle, the arrangement providing a basis for movement by barbels lacking an internal musculature (Benjamin, 1990). Active movement of barbels therefore, would of necessity be determined by the presence of an intrinsic or extrinsic musculature, or both, suitably innervated by their associated cranial nerves.

172 by slips of muscle from the pars supercialis (Singh, 1967). Varicose sensory nerve endings were located by Ono (1979) in the connective tissue at the base of the prectoral n rays of the gurnard, Aspitrigla cuculus and in the perichondrium of the barbel of the goatsh Mullus surmuletus. The barbel of Mullus, without an intrinsic musculature, has its perichondrium attached to a cartilage rod. Nerve endings of the hyomandibular branch of the facial nerve are considered to be proprioceptive, to monitor the position of the n rays and the barbel. Proximally, near the base, each member of the pair of barbels of Polymixia lowei is supported by three modied branchiostegal rays (from the hyoid arch), which articulate with the ceratohyal. Uniquely, within and along the barbel, transversely disposed semicircular striated muscle plates are arranged as a single column, each plate carrying 1624 muscle bres in two layers. Each muscle bre has an average diameter of 9.2 m with the sarcomere length 1.6 m. Muscle layers are separated by connective tissue and a large nerve, of two sets of different sized myelinated bres alongside the muscle, innervates it on proceeding distally. A large blood vessel extends between the barbel muscle and nerve components. Presumably, movement of the Polymixia barbel involves its intrinsic musculature. Unencapsulated free nerve endings, or beaded terminals, within the tendons of the third branchiostegal ray, were not assciated with the intrinsic muscles of the barbel, The n ray nerve endings of Polymixia were considered by Ono (1982) to be proprioceptive, like those in the pectoral n rays of Aspitrigla and barbels of Mullus, mechanoreceptive to stretch. The third branchiostegal ray acts as a sensory co-ordinator, to monitor the position of the barbel; the other branchiostegal rays function as supporting structures. The barbels of Mullus are highly mobile and can move independently, presumably effected by extrinsic muscles, like the movements of the n rays of Aspitrigla. in some way akin to a barbel form, is the rostrum of the freshwater Mastacembelidae, the spiny eels. Mastacembelis has a small eshy, anterior rostrum, relatively simple in cross-section without any supporting skeletal stuctures. A larger rostrum of Macrognathus, a continuation of the upper jaw and opening into the mouth ventrally, is lined on each side by a series of laterally expanded tooth plates: the maxillary bone is in continuity with the plates, though not part of the rostrum. Elongate ducts lead from paired terminal nostrils to the olfactory organs beyond the rostrum (Roberts, 1980). In Mastacembelis the rostrum may function in some way as a food sensory detector, perhaps mainly olfactory. In Macrognathus, in addtion the enlarged rostrum collects insect larvae and oligocoetes for feeding, a function perhaps related to the fact that some species burrow in the substrate during the day, or for longer periods during the dry season (Su, 1956). Barbels are believed to have several functions, though some views are purely speculative. The more general and reasonably likely view is that they are chemosensory and tactile organs mainly concerned with feeding. However, as only the nuptial males of Pimephales notatus have barbels, they may, in this case at least, play a role in reproduction or courtship, of sexual recognition (Gilbert & Bailey, 1912). The barbels of Rhinichthys cataractae may function in orientation towards a source of water-borne chemicals, or in intraspecic communication (Schmidt, 1983). Long ago Wright (1884) considered that barbels of shes were little else than modied projections of the skin, stiffened by cartilage, that increased the functional range of the epideral end buds. Because of the widespread presence of these end buds in barbels, the key, therefore, to understanding barbel function should relate to the functional activity of the so-called taste buds and the properties of the nerves supplying them: in adition other cellular components of the skin of barbels could well contribute to their functional activity. Jobert (1872) and Wright (1884), believed that the barbels, via their end buds, were tactile organs. However, since Herrick (1903), the prime function of the barbels was considered to be of gustation, a chemosensory property of the taste buds for the location and determination of the palatability of food (Finger, 1988). All external taste buds of shes, including those of the head and barbels, are innervated by cranial nerve VII (facial); those of the pharynx and palate are sup-

Functional activity of barbels First it may be noted that in addition to barbels, other elongate tentacular structures occur in the head region of some shes, for example the elaborate illicia of the Lophoformes, derived from ns to lure prey into the mouth. Another head structure of interest,

173 plied by nerves IX (glossopharyngeal) and X (vagus). A comuinis system includes specialized nerve bres to the viscera and highly differentiated bres to the lips, outer skin and oral cavity: an acoustic system is related to the lateral line neuromasts. The communis system is centred in the geniculate ganglion: distal to it, cutaneous and lateralis nerves join and proximal to it, gustatory bres terminate in the medulla (Herrick, 1901, 1903). A large facial lobe to control taste organs (and touch) in the barbels and jaws of shes, has since been conrmed (see Evans, 1940; Biedenbach, 1973; Kapoor et al., 1975; Finger, 1983, 1988). The size of the medullary gustatory lobes relates to the extent of their supply to the taste buds (Bhimacher, 1935, 1937). Fishes feeding in turbid waters usually have a high number of cutaneous taste buds, with an enlarged facial and reduced optic lobe. Fishes feeding in clear water, seeking food mainly by sight, have fewer cutaneous taste buds and large optic lobes (Davis & Miller, 1967): nocturnal feeders generally are similar (Evans, 1940; see also Mookerjee et al., 1950; Moore, 1950; Khanna & Singh, 1966). In general, shes with barbels are bottom-dwelling forms (Suyehiro, 1942). Some catsh monitor a considerable volume of water with their barbels, at the bottom of their habitat (Sterba, 1962), somewhat similar to that performed by the long n rays of the gurnard, Trigla (Steven, 1930), and the burbot, Lota lota monitoring food (Cochran, 1987). Mullet may dig into the sand with their chin barbels in search of food (Whitear, pers. comm.). There is neurophysiological evidence for chemoreception by taste buds (see Teeter & Brand, 1987). Chemoreception has been found to occur at the apical microvillous surface of the sensory cells, where amino acids and protein substances bind. In vivo and in vitro experiments, performed on the maxillary barbels of Ictalurus punctatus and Anguilla japonicus revealed a high degree if sensitivity to these substances (Caprio, 1975; Tucker, 1983). The stimulus to the barbel taste buds, certainly of great complexity whatever its nature (see Teeter & Brand, 1987), presumably is interpreted in the relevant centres in the brain (Tateda, 1964); Bardach et al., 1967, 1969; Bardach & Atema, 1971). Further support for chemo-sensitivity in barbels appeared from immuno-cytochemistry. Antibody G10 inhibits binding of L-alanine on catsh maxillary and mandibular barbel taste bud epithelium. The G10 antigen is present on the external surface of the microvilli of receptor cells, and this is associated with the taste receptor proteins of taste buds (Yonchek et al., 1987). In addition to chemo-sensibility, taste buds are considered to be multisensory (Hirata, 1966) and they can change function from chemo-reception to mechano-reception, termed a Wechelsinnesorgane (Kolmer, 1927). There is also rm evidence that barbels are mechanosensory. Indeed, nerves in the barbels of Ictalurus punctatus contain trigeminal tactile sensory bres as well as gustatory ones (Finger, 1976.) Barbels of Pristiophorus japonicus (Sato, 1937d) and Mystus vittatus (Agarwal & Rajbanshi, 1965) lack taste buds and their barbels were described as tactile structures. The presence of Merkel cells in barbel skin of some shes (Whitear, 1989) and free nerve endings also (Reutter, 1971) lends credence to this view. It has been advocated that basal cells of taste buds of some shes function as mechanoreceptors (Reutter, 1987), stimulated mechanically by friction between the plasma membrane and the basal lamina so that the basal cells function as paraneurones (Toyoshima et al., 1984). Wright (1884) believed that the end buds of the barblets of Ameiurus catus were tactile organs. Bateson (1890) reported these sense organs in a number of shes, for example in barbels of the pouting Gadus luscus and the rockling Ciliata mustela. Some sh feed by sight and smell but also use touch by the barbels to locate food. Agonus cataphractus, however, feed by sight, though having chin barbels. Among bottom-dwelling shes, the pouting and cod appear to use their barbels either as tactile or gustatory organs, snapping at food nearby on or off the bottom (Steven, 1930). The maxillary barbel, especially the middle third of Ameiurus (Ictalurus) nebulosus, is extremely sensitive to mechanical stimuli, judged from stimulation by currents of water or stroking the skin. Tactile receptors were believed by Hoagland (1933) to be involved. Chemo-sensitivity is less evident; the amplitude of the impulses, from stimulation of the barbel and lips by acetic acid, salt and sugars, was less than 10% of that elicited by mechanical stimulation. Hoagland (1933) concluded that differences in axon and neurone size were related to the specic sensibilities of the sense organs of barbel skin: indeed the nerve components of the Gasserian ganglion associated with tactile reception are larger than those from the geniculate ganglion related to the taste buds.

174 Biedenbach (1971) described barbels of Ictalurus nebulosus as feelers, that monitor food by contact; the response is fast and precise. Near the bottom of the lake, the maxillary and mandibular barbels glide over the surface, touching it and any available food Tactile sensibility was presumed to act via the taste buds and the facial nerve and by the epidermis, innervated by the trigeminal. Both sets of nerves enter the brain together: thereafter they separate, leading to their respective lobes. Biedenbach (1971, 1973) considered that the response of neurones in barbel skin to mechano- and chemo-sensory stimulation revealed that a majority of them were mechano-sensory and that only a small fraction respond to chemical stimulation. Furthermore, the responses of these sensory systems were intermingled and thus the enlarged facial lobe cannot be concerned exclusively with chemo-reception. The evidence implies that the individual sensory bud of barbel skin includes a high degree of tactilesensibility. In general, therefore, it is considered likely that barbels serve for gustation by chemosensibility, via the taste buds and also tactile sensibility, via the taste buds (see Kotrschal et al., 1991)and the Merkel cellnerve unit and free nerve endings in the epidermis. Details of the exact functioning of the different barbel components, especially of the taste buds, still need clarication (Teeter & Brand, 1987) (see Table 3 for the main features of structure and function of shes (vide supra), and those of amphibians and Erpeton among the reptiles (vide infra).

Figure 10. Micrograph of transverse section of the tentacle (near the tip) of a Xenopus laevis larva at NF stage 58. capillary; B basal epidermal cell; C cartilage; M melanophore; S surface epidermal cells; DF and VF dorsal and ventral surfaces of the tentacle. (X 660).

Tentacles of anuran larvae Tentacles are rare in anurans. Among the Pipidae, they occur in larvae of Xenopus laevis (Nieuwkoop & Faber, 1956), X. tropicalis Sokol, 1977) and X. gilli (Rau, 1978), but not in Pipa carvalhoi and Hymenochirus boettgeri (Sokol, 1977). In Xenopus laevis, for example, they originate early in larval ontogeny, at Nieuwkoop and Faber (NF) stage 44 (3 days 20 h old; 7.88.5 mm long). Short tentacular processes in NF stage 46 (larva 912 mm long), reach full development in NF stages 5055 (hind limbs developing); they regress at climax (NF stage 60) and have gone before the end, by NF stage 63 (Nieuwkoop & Faber, 1956). The prominent, slender, rm but exible tentacles, of maximum length 24 cms and 0.30.4 mm in dia-

meter, extend from the latero-frontal region of the head. Each tentacle has a two-layered non-cornied epidermis, whose surface has short microridges or microvilli and mucous vesicles. A central core of connective tissue surrounds a rod of hyaline cartilage (like many barbels of shes) and there are capillaries, broblasts, occasional melanophores and nerves (Figure 10). Collagen, situated directly below the epidermis, is not organized orthogonally. The cartilage is reported to be associated with fast and slow striated intrinsic muscles, distinguished by their banding, sarcotubular and mitochondrial content and motor end plates (Ovalle, 1976). Cannone & Kelly (1977) reported a small extrinsic muscle inserted on the proximal base of the cartilage (where it branches). When the muscle contracts, the tentacle is withdrawn into the lateral region of the head. The basal epidermal cells of the tentacle, without Figures of Eberth (Fox, 1992), contain tonolaments, mitochondria, free ribosomes and a scattered rER. Between the layers of epithelial cells, elliptical attened Merkel cells, each with a lobulated nucleus, have their long axis oriented parallel to the longitudinal surface of the tentacle (Ovalle, 1976, 1979). Merkel cell structure generally conforms to that in other amphibians (Fox & Whitear, 1978) (Figure 11). Immature Merkel cells are rst recognized in the epi-

175
Table 3. Summary in tabular form of the general structure, innervation and function of barbels/tentacles of shes, amphibians and the aquatic snake Erpeton among the reptiles. + denotes the presence (at least in some cases) and the absence (or not yet reported) of specic cellular and skeletal components Fishes Chondrostei + ? + head + ? ? + + V ? VII ? passive ? Taste Tactile ?

Cyclostomes Barbels (Tentacles) Larvae Adults Location Taste buds Club cells Goblet Cells (Mucous Cells) Merkel cells Photophores Axial Skeleton Innervation (cranial nerves) Regeneration Movement Function + ? + head + + +V ? passive Taste Tactile ?

Teleostei + + + head + + + + + + + V ? VII

Elasmobranchs + ? + head ? ? ? ? + ?

+ ? passive & Vol. passive ? Taste tactile ? Tactile Lure prey (illicium) Reptiles Erpeton + + head ? +? ? Passive ? Tactile ? Chemosensory ? Lure pre ? Camouage ? Sex Ornament ?

Anura Barbels (Tentacles) Larvae Adults Location Taste buds Club cells Goblet cells (Mucous cells) Merkel cells Photophores Axial skeleton Innervation (Cranial nerves) Regeneration Movement Function + + head + + + V+VII Passive Vol. ? Tactile

Amphibians Urodela Apoda + + branch area +V Passive ? Muc. secret. Tactile ? + + head +V ? Vol. Tactile Chemosensory ?

176 The tentacles are innervated by branches of the deep ophthalmic, maxillary and mandibular trigeminal cranial nerve (Patterson, 1939; Cannone & Kelly, 1977). Myelinated axons (517 m in diameter) along the tentacle, branch repeatedly, lose their myelin and Schwann cell coverings on entering the epidermis and terminate there as free nerve endings or synapse with Merkel cells (Figure 11). The full innervation of tentacles provides a basis for a tactile mechanoreceptive function (Cannone & Kelly, 1977). There appears to be little information on the regenerative ability of Xenopus tentacles. As in the case of balancers (vide infra), it is likely that they do not regenerate after amputation, at least when fully grown.

Balancers of urodelan larvae Balancers are slender rod-like appendages, on each side of the head of some urodele larvae. They are lacking in members of the Plethodontidae, Cryptobranchidae and in Ambystoma mexicanum, are rudimentary in Ambystoma tigrinum and some salamanders, but generally are well developed among the Ambystomidae, Salamandridae and Hynobidac (Harrison, 1925). The name arose from the belief that these organs propped up the head, to prevent the larva falling on its side before the fore-limbs develop. Typical examples are found in Ambystoma maculatus and A. punctatus (Hamburger, 1950) Triturus cristatus and Pleurodeles waltl (Fox, 1955, 1985a) (Figures 1216). Bell (1907) described the balancer of Diemyctylus viridescens to arise in a 45 mm embryo and last about two weeks. Balancers of Ambystoma tigrinum, rst visible externally at Harrison (H) stage 33 (before the external gills develop), reach maximum size by H stages 3839 (tiny forelimb buds in the larva): they are short-lived and lost soon afterwards (Nicholas, 1924). Likewise, balancers arise in A. punctatum H stage 34, reach full size (1.11.3 mm long 0.14 mm thick) at H stages 4041 and have disappeared at H stage 46, when the larva has three well developed branched external gills on each side and three-toed fore-limbs (Hamburger, 1950). Balancers of Pleurodeles waltl rst appear at Gallien and Durocher (GD) stage 28 (larva 5.4 mm long, 30 h old). At GD stage 34, just before hatching, they are about 1 mm long, are half-size at GD stage 44 (larva 17.5 mm long, 36 days old) and have disap-

Figure 11. Electronmicrograph transverse through the distal region of the tentacle of Xenopus laevis at NF stage 58, showlng the presence of a Merkel cell and associated nerve. M, Merkel cell in the epidermis; N, nerve bre against the Merkel cell surface. (X 11200). (Figures 10 and 11 courtesy of W. Eglmeier 1987, Anat. Embryol. 176).

dermis at NF stage 46 (larva 912 mm long, 4 days 10 h old), when three out of four of them contact the basement membrane. Their number has increased a day later, by NF stage 47 (Tachibana et al., 1980). Merkel cells in the tentacles vary in location, shape, content, structure and nerve association during development: probably they derive from epidermal cells (Eglmeier, 1987).

177

Figure 12. Larvae of Triturus cristatus carnifex 9.5 mm long (dorsal view) (a) and 9.0 mm (ventral view) (b) (just hatched); and T.c.karelini 9.5 mm long (dorsal and ventral views) (c,d) (24 h after hatching). These urodele larvae typically have well devloped anterior paired balancers and three pairs of external gills. (From H. Fox 1955, Copeia No. 2).

peared at GD stage 46, when the fore-limbs have four digits. Balancers of Hynobius fuscus, rst seen in larvae 6.57 mm long, reach maximum size (2 mm long) in the 16 mm larva: they disappear when the larva is 19 20 mm long (Murayama, 1928). The balancer is covered by a two-layered epithelium, enclosing a mesenchymal matrix, capillaries and nerves: a club-shaped thickening in front secretes mucus (Harrison, 1925). At an ultrastructural level, in Ambystoma opacum and A. jeffersonianum at H stage 34, outer cuboidal and inner columnar cells, joined by desmosomes, overly an adepidermal membrane. The balancer lengthens probably mainly by cell elongation. By H stage 36, the basal cells contain ribosomes, rER, mitochondria, pigment and residual yolk and lipid. Outer cells, with surface microvilli and a few cilia, contain randomly oriented tonolaments (seen later in basal cells), a Golgi complex and multivesicular bodies. Hemidesmosomes occur on the proximal basal cell margin. Below the adepidermal membrane, collagen layers have little orthogonal arrangement (Anderson & Kollros, 1962). Likewise, surface balancer cells of the Pleurodeles larva have a microvillous surface with occasional cilia, an extensive rER (often in whorls), a well developed

Golgi complex and a heavy content of mucous granules. There is a pronounced surface layer of mucus (Fox, 1985a) (Figure 13). The balancer is innervated by a small nerve from the Gasserian ganglion and vascularised from the hyomandibular artery and jugular vein, which form a single loop. Blood is rst seen in the balancer of Ambystoma at H stage 37 (Kollros, 1940). Balancers degenerate by autolysis (Figure 6), via lysosomal enzymes; lost either by constriction at the base (autotomy), as in Diemyctylus (Bell, 1907), Hynobius (Murayama, 1928) and Ambystoma punctatum (Harrison, 1925), or resorption, as in A. tigrinum (Nicholas, 1924), or shrivelling, as in A.opacum (Kollros, 1940) and Pleurodeles (Gallien & Durocher, 1957). Future balancer tissue of the embryo is induced by lateral plate mesoderm. In Ambystoma, prospective balancer ectoderm transplanted to other regions of the body, after neurula H stage 28, will form a balancer, and it is thus determined after this stage (Harrison, 1925). There is little or no regeneration after partial transection (Bell, 1907; Nicholas, 1924), Its life span would appear to be controlled by intrinsic factors, for balancers transplanted between young and older specimens and vice versa showed the graft to disappear

178

Figures 1315. Figure 13. Surface of a balancer of Pleurodeles waltl larva at Gallien and Durocher (GD) stage 32 (larva 7 mm long), showing a prominent layer of mucus (Mu) up to 5 m thick. (Scale mark of electronmicrograph (TEM) 1 m). Figure 14. Nerves in the epidermis of a balancer of P. waltl at GD stage 37 (larva 11.8 mm ong, forelimbs palette-shaped). The Schwann cell sheath around the nerve is clearly recognizeable: usually this sheath is absent from nerves in the amphibian epidermis. BC, basal cell of the epidermis; BL, basemcnt lamella collagen of the dermis; N, nerve bre; SCS, Schwann cell sheath. (Scale mark of TEM 0.5 m). Figure 15. Basal region of the balancer epidermis of P. waltl at GD stage 38 (larva 12 mm long, rst feeding stage). There are 12 neurites in this part of the epidermis, an example of the extensive innervation of this structure. (Scale mark of TEM 1 m).

179 at about the same time and stage as control balancers, and they are not inuenced by the host (Nakamura, 1936; Kollros, 1940). Balancers were considered to be respiratory organs (looking like external gills, Spallanzani, 178489), adhesive, mechanical and mobile organs, though indeed a sensory function was advocated (Gadow, 1909; Cunningham, 1912). However, an epidermis with an extensive rER, mucous granules and a surface of mucus, suggests a mucus-secreting function. Cement gland cells of Xenopus embryos have a similar structure and secrete a glycoproteinaceous mucus (Perry & Waddington, 1966). Possibly balancer surface mucus assists adherence to aquatic ora and aids balance. However, in Pleurodeles larvae, for example, balancers may well have a sensory function also, for they are innervated extensively by the trigeminal nerve; up to 12 branches of unmyelinated nerves may be grouped together between the epidermal cells. In one rare instance, a nerve with a Schwann cell sheath was found in the basal layer (Fox, 1985a) (Figures 14, 15). The skin of the head (and body and tail), of the embryonic and larval Xenopus, is innervated by naked sensory neurites, from the cranial and Rohon-Beard cells of the nerve cord (Hayes & Roberts, 1983). In the newly-hatched Xenopus, or when the tadpole hangs by a mucus thread, stimulation of the cement gland receptors, by touch, inhibits swimming: the sensory neurites to the gland, acting through the central nervous system, are responsible for this effect (Roberts & Blight, 1975). The somewhat similar morpho-physiological arrangement in the balancer of the Pleurodeles larva, may well operate in a like manner, though other sensory functions cannot be ruled out. The fully developed tentacle extends from and retracts into the sheath, which has the peripheral components of the orbital Harderian glands at its base (Badenhorst, 1978; Billo & Wake, 1987). The tentacle is vascularized by branches of the stapedial and carotid arteries and drained by branches of the jugular vein. Retraction is effected by retractor tentaculi muscles derived from the extrinsic eye musculature, which is innervated by the cranial ramus abducens VI. The tentacle itself receives branches from the trigeminal nerve. Tentacles of Ichthyophis kohtaoensis and I. orthoplicatus, for example, are 35 mm long, each bounded by an epidermis of veseven cellular layers, with a cornied surface 2.54 m wide. The epithelial cells of the stratum intermedium, joined by desmosomes, contain among other things smooth-surfaced vesicles and occasional multivesicular bodies, polysomes,a Golgi complex and tonolaments: mitochondria and rER are rare. Basal cells, oriented roughly at right angles to the skin surface, have an indented irregular proximal margin with poorly developed hemidesmosomes. They overlay an adjacent adepidermal membrane and space. Basal cells, with bundles of tonolaments that lead perpendicularly into the cell from the proximal margin, are separated by electronlucent material of unknown nature: within this basal layer are immigrant leucocytes (Figures 18, 19a, b). Merkel cells and ask cells were not seen in the tentacle epidermis, though they are present in the epidermis of body skin (Fox, 1983, 1986b, 1987; Fox & Whitear, 1978). The epidermis of the tentacle is extensively innervated, at all levels, by intercellularly located non-myelinated nerves. The dermis and central area of the tentacle show collagen, capillaries, broblasts, granulocytes, melanophores and laminophores and unmyelinated and myelinated nerves, the latter up to 8 m in diameter (Figures 19a, b). There are no dermal scales, in contrast to their presence in the body (Zylberberg et al., 1980), but at the base of the tentacle, adjoining the head, incipient scale structures appear to delineate the region where the tentacle meets the head. In the dermis of the tentacle, small mucous glands, each with a duct, are bounded by a myoepithelial sheath, that envelops peripheral mitochondria-rich cells and the swollen mucus-producing cells. Whether glands extend throughout the tentacle or only occur towards the base, is not clear (Fox, 1985b). Billo & Wake (1987) described the structure and development of the tentacles and associated organs

Tentacles of apodans Adult apodans possess a pair of tentacles (Figure 17), each one in a sheath (or sac) behind the nostril, midway between the eye and external naris (Taylor, 1968). Since their discovery by Leydig (1868), aspects of their structure, histology, innervation, vascularity, development and phylogeny have been described (see Billo & Wake, 1987). Features of tentacle ne structure, especially that of its skin, have been detailed (Fox, 1985b). Tentacles originate at metamorphosis, when there is keratinization of the epidermis and loss of the lateral line organs (Wake, 1977).

180

Figure 16. Balancer epidermis of a larva of P. waltl at GD stage 38 showing an extensive area of degeneration in a basal epidermal cell. Soon afterwards, at GD stage 41 (larva with three digits to the forelimb), some balancers have disappeared or are merely degenerate stumps. (Scale mark of TEM 2 m). Figures. 13l6 from H. Fox 1985a, Acta Zool. 66).

of Dermophis mexicanus and Gymnophis multiplicata, throughout a comprehensive series of embryo, foetal, juvenile and adult forms, ranging from 5 to 30 mm (embryos) to >250 mm total length (adults). The tentacular sheath encloses most of the tentacular apparatus, that is the tentacular fold, Harderian gland, eye muscles and nerves. The Sarasins (18871890) suggested that the tentacular sheath originated from an epidermal sensory groove, into which the Harderian gland discharged mucus: or that it is an enlarged common duct of the Harderian gland with the tentacular fold a secondary formation, a view generally supported by Badenhorst (1978). Billo & Wake (l987), however, propose that the tentacle originates from modied eye components; that the tentacular fold and lower eye lid region

of amphibians are homologous; that the conjunctival sac and the tentacular sheath are likewise homologous and the conjunctiva as a whole is the homologue of the tentacular sac. Furthermore, the tentacle aperture, through which the tentacle protrudes, corresponds to the interpalpebral space. Apodans are mainly subterranean and in this habitat the tentacles probably function as sensory organs (Taylor, 1968). Their ne structure and extensive innervation lend support to this view, though the specic nature of any sensory function, whether chemo- or mechano-sensory, or both, has yet to be elucidated (Fox, 1985b).

181

Figures 1719. Figure 17. Head of an adult Ichthyophis kohtaoensis (about twice the size) showing the small everted tentacle. (Picture courtesy of W. Himstedt). Figure 18. TEM of the outer region of the tentacle of an adult Ichthyophis. cc, cornied epidermal surface; N, nucleus of epidermal cell (second layer); PNR, less dense perinuclear area of cell. The second and third layers include cells with a high content of tonolaments. Figure 19. (a) Nerves in the epidermis of a tentacle of Ichthyophis arising from nerves in the dermis of (b) The nerve in the dermis is unmyelinated with a Schwann cell sheath. AM, adepidermal membrane; BC, basal cell of the epidermis; BN, branching nerve; CO, dermal collagen; Derm, dermis; Ne, nerve bre; NeB, nerve bundle. (Figures 18 and 19 from H. Fox 1985, J. Zool. Lond. 205).

182

Figure 20. Harpsesaurus beccari. (A) Before feeding; (B) Immediately after seizing prey. Note the pronounced rostral appendage. (Courtesy W. Bhme 1989, Tropical Zool. 2).

Tentacles of reptiles A number of reptiles have appendage-like organs of uncertain function, projecting from the head. There are large scaly projections on the snout of some agamid lizards, for example in Harpesaurus beccarii (Figure 2O) which may be concerned in species recognition of sympatric forms (Bhme, 1989). The Madagascan snake, Langaha allueda, has a single projection from the snout, supercially similar in structure to the tentacles of Erpeton, which may act for camouage (Bellairs, 1969; Hahn, 1973). Vipera ammodytes has a large mass of cavernous tissue at the base of a single pointed projection of the snout, presumably able to erect the appendage.

Appendages of chelonians Winokur (1982a) described appendages (termed barbels in the gular region) and tubercles (smaller and less elongate than barbels in the neck region), in four families of chelonians, the Chelydridae, Kinosternidae,

Pelomedusidae and Chelidae. These appendages, or elongate protrusions of the keratinized and often pigmented epidermis and dermis, are without neuromasts, taste buds and Merkel cell-neurite complexes: they also lack skeletal structures, muscle and erectile tissue. However, collagen is present in the dermis and they are highly innervated by small free nerves. Apart from some kinosternid barbels and tubercles, most of these appendages are not highly vascularized, though the long tubercles near the base of the neck of Pelochelys, a trionychid, have large blood vessels. The gular barbels are particularly prominent in the chelid Phrynops geoffroanus: in Malaclemys temmincki of the Chelydridae, gular barbels of hatchlings and juveniles may be 510 mm long, though in larger specimens they are reduced in length. Appendages are most elaborate in Macroclemys temmincki and in Chelys mbriatus (Mata mata, Hartline, 1967) (Chelidae). Gular barbels occur in pairs, often in rows. Likewise, tubercles frequently occur in rows on the lateral

183 regions of the neck. There is no sexual dimorphism with these organs. Chelonian appendages would seem likely to serve for mechanoreception (Hartline, 1967), detecting currents in the water, or they act as touch receptors: other functions could be for camouage, or aquatic respiration by increasing the skin surface area, or for participation in courtship by touching between sexes, as in some Australian chelids, or in some manner they serve for protection, or bodily orientation. The subject, together with earlier literature, was reviewed by Winokur (1982a). Possibly all chelonian integumentary appendages are homologous and derived from the rows of (ossied) tuberoles found in ancestral forms. There appears to be no relationship between carnivory and the degree of development of the barbels, among these chelonians. It is of interest that the herbivorous Podocnemis unilis (Pelomedusidae) has a single gular barbel, possibly derived by fusion of a pair, a development also seen in Elseya dentata (Chelydae) (Winokur, 1982a) and likewise found in barbels of exocoetids among the teleosts (vide supra). Among chelonians, the Carettochelydae, Trionychidae, Pelomedusidae and Chelidae include species that possess nasal erectile tissue with extensive smooth muscle, within the snout, that act on the internal diameter of the nasal passage. The carettochelyds and trionychids can alter the angle of the tubular snout relative to the head. The eshy snout of these chelonians is of importance in drawing clear water into the mouth, when they burrow into the substratum. The trionychids and some carettochelyds, have highly vascularized, liform pharyngeal papillae that presumably function in respiration (see Winokur, 1982b).

Figure 21. Erpeton tentaculatum, an aquatic Asian water snake, showing (A) the head protruding from the water with its accid tentacles; (B) the same specimen with erect tentacles. (From R. M. Winokur 1977, Herpetologica 33).

Tentacles of Erpeton The aquatic ovo-viviparous colubrid Erpeton tentaculatum, commonly called the shing snake, from Indochina and neighbouring countries, is unique among snakes in possessing a pair of blunt scaly appendages, or tentacles (Lange, 1931; Hahn, 1973; Winokur, 1977), situated laterally in front of the snout (Figures 2lA, B). They are 56 mm long (about 1/6 the length of the head), and covered with scales that are slightly smaller than others on the head. The keratinized epidermis is underlain by a loosely organized stratum laxum and a deeper more organized stratum com-

pactum. Hahn (1973) reported the absence of muscles and nerves in the tentacles, but Winokur (1977) described a subcutaneum of loose areolar connective tissue, with smooth muscle bres extending longitudinally in the tentacle and anchored to the stratum compactum. Melanophores occur in the stratum laxum, compactum and the subcutaneum. Large nerves extend parallel to adjacent blood vessels and naked nerve terminals occur in the epidermis, and occasionally in the stratum laxum, near the dermo-epldermal junction. Earlier workers (see references in Hahn, 1973) considered that the tentacles detected food in the water; that they were muscular and acted as a lure for

184 unwary sh (Parker, 1963); or they serve for camouage and are ornamental (Shaw, 1965) perhaps of sexual nature (Hahn, 1973. The tentacles point forwards when the snake is submerged but are laid back and accid when the head is above the water surface (Figure 21A, B). If the snake is disturbed the tentacles become erect, so presumably they respond to external stimuli: possibly they function as mechanoreceptors for they are highly innervated, perhaps to detect vibrations in the water, especially of likely prey (Winokur, 1977). pairs of barbels are reduced to a pair of minute maxillary barbels. In exocoetids, paired barbels on the chin fuse into a single barbel (Collette et al., 1984). Barbels can regenerate after amputation, the process primarily dependent upon the regenerating barbel nerves, the presence of chondroblasts from the perichondrium and a requisite temperature. Likewise, taste buds are dependent on adequate innervation for their maturity, maintenance and function. Balancers and tentacles of urodelan and anuran larvae orignate early in ontogeny: balancers disappear in fairly young larvae; tentacles of anurans, such as Xenopus are lost during metamorphosis. Apodan tentacles originate after metamorphosis. Nothing appears to be known about their regenerative capabilities, or of those of reptiles including Erpeton.

Discussion The foregoing account of tentacular structures, in the head region of sub-mammalians, can be broadly summarised and from the evidence one can reach some reasonably sound conclusions. Clearly in these animals there is a variety of head projections covered by skin. In hemichordates and cephlochordates there are tentacular ciliated arms and oral cirrhi respectively; shes, in addition to the true barbels may have illicia, supraorbital cirrhi and oral papillae and in mastacembelids a terminal rostrum. Among amphibians, some larval anurans, for example Xenopus, have whiskers; many larval urodelan species have balancers and adult apodans have prominent tentacles. Among reptiles, only Erpeton, a water-dwelling snake, has pronounced moveable tentacles. In all these aquatic forms (only the adult apodans are subterranean), the tentacular structures located mainly around the mouth, doubtless receive oncoming stimuli, usually as the animal moves forward, or from currents in stationary forms, in dark silty waters near the bottom of the habitat. Their function is sensory, mainly involved in feeding, though the exact nature of the tentacular response is not always clearly known.

Mobility In terms of mobility and component musculature, tentacles of the different groups are variable. Movement of the barbels of myxinoids, elasmobranchs and chondrosteans is little understood. Whether it is passive or active, if it occurs at all, is not clear. Barbels of teleosts move passively or voluntarily by the use of extrinsic, or perhaps in some cases, intrinsic muscles. Tentacles of Xenopus appear to move voluntarily, motivated by extrinsic muscles; balancers are passive and apodan tentacles retractile, indeed are highly active, effected by an extrinsic musculature. Tentacles of Erpeton have intrinsic muscles and though usually passive, on occasion show voluntary movement.

Function A role for sh barbels as gustatory and tactile foodlocating structures is likely, for shes living in turbid waters. The evolution of nger-like barbels and other ap-like projections around the mouth, provided with sensory component cells, would be of selective advantage for shes seeking food where vision is restricted (Gilbert & Bailey, 1972). Barbels and n rays of teleosts are moblile structures in their aquatic environment: primarily these elongate structures extend the ranged of perception for feeding. Indeed, some shes with only a single small barbel, like Lota lota, have their analagous paired pelvic ns in a jugular position anterior to the pectoral ns, with their elongated n rays supplied with taste

Origin development maintenance and regeneration Barbels of silurid teleosts originate early, sometimes before hatching, those of cyprinids late in larval life. In some cases, for example among gadiforms and exocoetids, mental barbels originate in juveniles. During ontogeny, some barbels may disappear, as in the Indian catsh Silonia silondia, where the three

185 buds (Cochran, 1987). Taste buds are a common feature of such n rays as in rocklings Gaidopsarus and Ciliata (Crisp et al., 1975; Whitear & Kotrschal, 1986) and Aspitrigla (Ono, 1987) (see also Jakubowski, 1983; Jakubowski & Whitear, 1990). In teleosts, the initial water soluble chemical stimuli, of the gustatory cells of the barbels and n rays (see Caprio, 1988, are transmitted to centres in the hind brain and thence the ventral diencephalon (Lamb & Caprio, 1993), where they are integrated. Such cerebral activities (see also Kotrschal et al., 1991) albeit little understood, result in the sh directed towards the source of palatable food. Tactile stimulation of the barbels, via cerebral centres, likewise inuences directional activities of the sh. Indeed, chemoreception for example via olfaction and taste (Caprio, 1975) and mechanoreception in the skin, via nerves and Merkel cells, are major sensory features of terrestrial species. There appears to be little information, at least from electronmicroscopy and neurophysiology, on illicia. The most important feature of these structures is the bioluminescent light organ of photophores, at the tip. Angler shes generally are less active and the illicium lures unwary sh towards the mouth. Presumably there is then a visual response to locate and thence devour such prey, via activity of the jaws. Taste buds are widespread in the skin, tongue, mouth and pharynx of vertebrates: they are also a major multicellular component of sh barbels. However, according to Reutter & Witt (1993), taste buds may not have evolved progressively and conseculatively throughout the different vertebrate groups. Within each class, taste buds are highly specialized in structure and function and not enough is yet known about them to prepare a phylogenetic tree. Nevertheless, taste buds show similarity in form and content throughout the vertebrates; doubtless they have an ancient phylogenetic lineage. Barbels of teleosts, usually replete with taste buds (Reutter, 1986; Reutter & Witt, 1993), are of chemoand mechanosensory function, which together with sight and olfaction is concerned with feeding (Biedenbach, 1971, 1973). The availability, location and acceptability of food, or comparable chemical substances (see Tucker, 1983), are monitored by the barbel sensory cells,as peripheral agents of the brain (Caprio, 1988). The presence of free nerve endings and Merkel cells in barbels (Whitear, 1989), also implies a tactile function, an advantage to shes inhabiting dark regions, when direct contact with available food would be benecial (Biedenbach, 1971). Nevertheless, barbels of some teleosts may be without taste buds: some contain Merkel cells and presumably others are without them. The same goes for other cell types such as goblet and club cells, which vary in number and location, or are missing, in some barbels. Likewise, an axial skeleton may or may not occur in barbels of some specics: in this case connective tissue may play a supportive role. Variation in barbel structure thus strongly suggests a functional diversity in those of different barbeled forms, doubtless related to the mode of life of the individual. Orbital cirrhi of some teleosts, for example those of Hypsoblennius gilberti, have taste buds (von Bartheld & Meyer, 1985). Again, Azuma emniom and Hemipterus villosus have barbel-like processes with taste buds, that act as feelers in search of food (Sato, 1977b). Papillae on the head of Paragobiodon encephalus and oral disc papillae of the lampreys Geotria australis and Lampetra uviatilis, appear to be sensory structures of chemo and/or mechanosensibility. Tentacle function of chondrosteans and elasmobanchs is not clearly understood. Barbels of Acipenser ruthenus have taste buds, as shown long ago by Dogiel (1897). Presumably they serve for chemoreception and may also be tactile. Barbels of elasmobranchs, or at least some of them, are probably tactile, for those of Pristiophorus, for example, lack taste buds. Tentacles of the myxinoids Myxine glutinosa and Eptatretus burgeri have taste buds; probably they function as chemo and mechanoreceptors. Among amphibians, the presence of Merkel cells in the epidermis of the tentacles of Xenopus (Ovalle, 1979; Tachibana et al., 1980), and free nerve endings also (Eglmeier, 1987), argues in favour of a mechanoreceptive function for this organ (Cannone & Kelly, 1977). A variety of functions has been ascribed to urodelan balancers (vide supra), indeed the name infers a purely mechanical one. However, they secrete mucus, especially at the tip, so presumably they are adhesive. Again, they are extensively innervated by naked neurites, as seen in the balancers of Pleurodeles, so it is likely that they are also tactile (Fox, 1985a). Likewise, the epidermis of the tentacles of the apodan Ichthyophis is highly innervated by free nerves. A tactile function for these organs of the sub-

186 terranean forms seems likely, where vision is impaired (Fox, 1985b). The tentacles of chelonians and Erpeton may be mechanoreceptive, detecting vibrations in the water (Winokur, 1977; 1982a), though this view is still poblematical. this respect, while others are more specialized in their reduction or loss. It is clear that between the major groups of shes, amphibians and reptiles, barbels/tentacles are not homologous structures. Tentacles of Xenopus and balancers of urodeles have, among other things, been considered as homologues of external gills and their evolutionary relationships are vague. Apodan tentacles are believed by Billo & Wake (1989) to derive from eye structures, an extremely unlikely origin in the case of the tentacles of other groups. One may conclude, therefore, that barbels and tentacles, within the different major groups, are specialized organs that have originated sui generis and, at least in shes, a number of times. Furthermore, they are without any important phylogenetic signicance within and between the different groups. Further evidence on the subject, from palaeontology, is unlikely to be forthcoming and until more is known about the ontogeny of these tentacular structures, any apppraisal of their phylogeny, within each submammalian group, of necessity must remain purely speculative.

Homology and phylogeny The tentacles of the different groups, as so dened (vide supra), are outgrowths of the head that are suitably innervated; in teleosts by sensory and motor branches of the V and VII nerves and in those of the other groups, including myxinoids by nerve V. Barbels of teleosts are basically different in origin from other sensory structures, like elongate n rays and illicia, aibeit in some ways showing similarities morphologically and topographically. Barbels are not homologous with n rays and illicia. However, throughout the teleosts, true barbels within each family that has them, presumably are homologous in terms of ontogeny, location, structure and function. Oral cirrhi of some shes, of somewhat similar structure and function, may well be reduced or immature barbels. Orbital cirrhi, though located near the eyes, likewise could well fall into the same category. In terms of phylogenetic relationships, it is likely that barbels arose independently in shes (Howes, 1991), probably several times at least in siluroids and cyprinids (Gilbert & Bailey, 1972; Fink & Fink, 1981) and their presence or absence is of no great phylogenetic signicance (Cortes, 1968; Fahay & Markle, 1984). Among the ostariophysans, for example, barbels are considered to be a poor indication of evolutionary relationships (Fink & Fink, 1981; Schmidt, 1983). However, within a teleost order such as the Siluriformes, barbel origin and development, number and location, could be of some importance (Fuiman, 1984) and when taken together with other morphological characters might well provide further evidence of interfamilial or species relationships (Howes, 1991). That barbeled forms are more primitive than those without them (Arai, 1982) is unlikely, when other characters are taken into account (Howes, 1991). Nevertheless, barbels may be lost during ontogeny, as for example in Parasilurus asotus (Atoda, 1935) and Silonia silondia (Karamchandani & Motwani 1956). Thus some teleosts without barbels may well be primitive in

Summary Among shes barbels are present in myxinoids, elasmobranchs, chondrosteans and teleosts. Among amphibians, paired tentacles occur in adult apodans and in a few species of anuran larval Pipidae; there are are also paired balances in some species of larval urodeles. Among reptiles only some chelonians and the water snake Erpeton possess true tentacles. Fish barbels, of varied histological structure and with or without a supporting skeleton, are widespread in the teleosts. They are highly innervated and usually richly supplied with taste buds: Merkel cells, among other specialized epidermal cells, may also occur. Available evidence, mainly from teleosts, leads to the conclusion that barbels are chemo and mechano-sensory organs, mainly concerned with feeding especially in bottom-dwelling forms, locating and monitoring food by passive and active movements. Amphibian tentacles probably are mainly tactile, all of them (including those of Xenopus with Merkel cells) are highly innervated. Balancers secrete mucus and are also adhesive. Tentacles of chelonians and Erpeton may detect vibrations in the ambient water; they might be concerned with feeding, defence, serve for camouage, or for some other as yet unknown purpose.

187 Evidence from teleosts shows that barbels can regenerate after amputation and that growth and maintenance of structure and function are dependent upon an intact innervation. Between the different submammalian groups, tentacles are not homologous in terms of embryology (hardly known in most cases) and morphology, though there are some similarities in function. Fish barbels probably arose independently and a number of times within different lineages. They are a poor indication of phylogenetic relationships, possibly only of value when considered together with other more signicant morphological characters.
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Acknowledgements Thanks are due to: Mary Whitear and Colin Patterson for advice and information on the subject, especially on the shes and to Carl Gans for his comments on the reptiles; to Frances Mussett and Jill Bailey for help in seeking reference literature and Pat Ferguson for photographic work. The following kindly supplied photographs, negatives or reprints, or gave permission to use illustrations of their published work: Wolfgang Bohme, Wolfgang Eglmeier, Werner Himstedt, Robert Patzner, Klaus Reutter, Mitsuo Sato, Robert Winokur and Marvalee Wake. Their generosity is much appreciated. Permission to use various illustrations in the work from the publishers of the following journals is warmly acknowledged. American Society for Ichthyologists and Herpetologists (ASIH), Illinois (Copeia); Editrice Sedicesimo (Tropical Zoology); Ichthyological Society of Japan (Japanese Journal of Ichthyology); Pergamon Press, Oxford (Acta Zoologica, Zoologica Scripta); Society for Systematic Zoology, Herpetological League, Louisiana (Herpetologica); Springer Verlag, Heidelberg (Cell Tissue Research, Biology of the Integument) Zoological Society of London (Journal of Zoology). I am especially grateful to John Cloudsley Thompson for his help in seeing the work through to publication.

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