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Luhman, 1935 (Digenea: Spirorchidae), with Comments on Other Species in the Genus
Author(s): Thomas R. Platt and David Blair
Source: The Journal of Parasitology, Vol. 84, No. 3 (Jun., 1998), pp. 594-600
Published by: Allen Press on behalf of The American Society of Parasitologists
Stable URL: https://www.jstor.org/stable/3284729
Accessed: 25-01-2019 17:33 UTC
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J. Parasitol., 84(3), 1998 p. 594-6(X)
? American Society of Parasitologists 1998
ABSTRACT: Hapalotrema mistroides (Monticelli, 1896) Stiles and Hassall, 1908 and Hapalotrema synorchis Luhman, 1935 are
redescribed using specimens from the loggerhead turtle, Caretta caretta (L.). The redescription of H. mistroides is based on
specimens collected by Looss and described as Hapalotrema constrictum Leared, 1862 and renamed Hapalotrema loossi Price,
1934, which is now considered a junior synonym of H. mistroides. Hapalotrema orientalis Takeuti, 1942 is considered a junior
synonym of Hapalotrema synorchis. The redescriptions are consistent with the originals but provide an unreported range of
variation while adding new information about the reproductive systems. Reexamination of Hapalotrema dorsopora Dailey, Fast,
and Balazs, 1993 confirms the presence of a reproductive system typical for the genus and the absence of a dorsal genital pore;
therefore, H. dorsopora is reduced to a junior synonym of Hapalotrema mehrai Rao, 1976. Four valid species of Hapalotrema
are recognized: H. mistroides, H. synorchis, H. postorchis, and H. mehrai, and a key to the species is provided.
As currently constituted, the genus Hapalotrema Looss, 1899 H. dorsopora Dailey, Fast, and Balazs, 1993, holotype (USNPC 82326),
paratype (USNPC 82327); Hapalotrema postorchis Rao, 1976, voucher
(Digenea: Spirorchidae) contains 8 species reported exclusively
(USNPC 82324, Dailey et al. [1993]); H. synorchis Luhman, 1935,
from the circulatory systems of marine turtles (Smith, 1997). holotype (USNPC 8909), and vouchers (USNPC 73323, Fischthal and
The discovery of specimens of Hapalotrema spp. from turtles Acholonu [1976]). Additional specimens from the junior author's col-
off the coast of Australia prompted a reassessment of Hapalo- lection were used, as was information from published descriptions.
trema mistroides (Monticelli, 1896) and Hapalotrema synorchis Numerous specimens of spirorchids have been collected from marine
turtles by the junior author during the past 2 decades. Many of the
Luhman, 1935.
turtles were examined opportunistically and some had been dead for
Price (1934) recognized significant nomenclatural problems undetermined lengths of time before necropsy. Methods of killing and
involving species assigned to both Hapalotrema and Learedius fixation varied with circumstances. Specimens were stained in Mayer's
and proposed several changes to rectify the situation. The hematoxylin, following standard procedures, cleared, and mounted in
names applied to species of both genera sensu Price (1934) Canada balsam as whole mounts for microscopic examination.
The following measurements are used in species descriptions: genital
have become the standard for the past 60 yr. We feel that Price
pore/TL = distance from the anterior end to the genital pore/total length
erred in several of his decisions (Platt and Blair, 1996), but that
and presented as a percentage; forebody/TL = distance from anterior
strict application of the rules of zoological nomenclature end to body constriction/total length and presented as a percentage.
(Anonymous, 1985) would not be in the best interests of no- Drawings were made with the aid of a drawing tube. Measurements are
menclatural stability. The International Commission for Zoo-in micrometers unless otherwise stated and presented as the range fol-
lowed by the mean in parentheses.
logical Nomenclature exercised its plenary power to recognize
Hapalotrema loossi Price, 1934 as the type species of the genus
and to retain the concept of Hapalotrema Looss, 1899 and DESCRIPTION
Learedius Price, 1934 as defined by Price (1934) (Anonymous,
Hapalotrema mistroides (Monticelli, 1896) Stiles and Hassall,
1997).
1908
Cribb and Gordon (1998) reexamined the status of several (Figs. 1, 2; Table I)
species of Hapalotrema and concluded that Hapalotrema dor-
sopora Dailey, Fast and Balazs, 1993 and Hapalotrema pam- Synonyms: Mesogonimus mistroides Monticelli, 1896; H. constrictum
banensis Gupta and Mehrotra, 1981 were junior synonyms of (Leared, 1862) Looss, 1899; H. loossi Price, 1934.
Hapalotrema mehrai Rao, 1976. It is our intention to review Diagnosis (based on 8 whole mounts and 1 sectioned specimen):
the remaining species of Hapalotrema, with particular attention
Body robust, maximum width in posterior /2 of body; division into
to the species commonly reported from the loggerhead turtle, forebody and hindbody indistinct, near acetabulum. Small tegumental
Caretta caretta. spines present anteriorly, diminishing posteriorly, absent posterior to
acetabulum. Oral sucker subterminal, wider than long; esophagus slight-
ly sinuous, expanded distally, surrounded by glandular cells at cecal
MATERIALS AND METHODS bifurcation. Intestinal ceca bifurcate at level of acetabulum, terminate
594
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PLATT AND BLAIR-REDESCRIPTION OF HAPALOTREMA SPP. 595
FIGURE 1-3. 1. Hapalotrema mistroides adult, ventral (scale bar = 1 mm); lectotype of Hapalotrema loossi. 2. Hapa
genitalia, ventral (scale bar = 250 am); lectotype of Hapalotrema loossi. 3. Hapalotrema synorchis adult, ventral (scale bar = 1 mm).
Type host: Caretta caretta, the loggerhead turtle. Monticelli's (1896) description of H. mistroides was not complete by
Other hosts: Chelonia mydas, the green turtle. current standards and our attempts to locate his specimens have been
Type locality: Mediterranean Sea near Naples, Italy (Monticelli, unsuccessful. Price (1934) noted striking similarities between Monti-
1896). celli's description and H. loossi. He preferred, however, to recognize 2
Other localities: Mediterranean Sea near Abukir, Egypt; Shark Bay, species based on several differences in the illustrations of the 2 forms:
Western Australia, Australia (present study; voucher specimens QM number of testes in the postovarial group, 16 in H. mistroides and 10
G214179-81 from C. caretta). in H. loossi; vitelline fields confluent anterior to the preovarian testes
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596 THE JOURNAL OF PARASITOLOGY, VOL. 84, NO. 3, JUNE 1998
TABLE I. Measurements of Hapalotrema mistroides (Monticelli, 1896) from the loggerhead turtle, Caretta caretta.
Character
Testis no.
in H. mistroides but not in H. loossi; differences in the sucker ratios H. loossi Price, 1934 and the remaining specimens listed in the Mate-
and the relative distances between the suckers in the 2 species. Neither rials and Methods from SMNH as paralectotypes. Considering the
of the original authors provided information on the range of variation strong similarities in the original descriptions of these taxa, the fact that
found in their specimens. both were taken from the same location in the same host species, and
Reexamination of Looss's specimens revealed 10-12 postovarian tes- that both turtles were taken in the Mediterranean Sea, we feel H. mis-
tes (Table I). Specimens of this morphotype from the type host collectedtroides should be considered a senior synonym of H. loossi, and H.
at Shark Bay, Western Australia, have 10-15 postovarian testes. Half mistroides becomes the recognized name for this species. The interested
of Looss' specimens show the anterior vitelline fields confluent anterior reader is directed to Platt and Blair (1996) for the nomenclatural details
to the preovarian testes, and the remainder probably would have, had and Anonymous (1997) for the ICZN ruling.
the specimens not been so mercilessly flattened.
Monticelli's (1896) figures 2 and 3 present distinctly different con-
DESCRIPTION
cepts of relative sucker size and sucker position. Figure 2 of Monticelli
(1896) shows the acetabulum larger than the oral sucker and the dis- Hapalotrema synorchis Luhman, 1935
tance between the suckers consistent with Looss' material. Monticelli's (Fig. 3; Table II)
(1896) figure 3 appears to be a caricature with the posterior portion of
Synonym: Hapalotrema orientalis Takeuti, 1942.
the worm greatly enlarged in order to present adequately the internal
organs, and the acetabulum and oral sucker are shown nearly equal in Diagnosis: Body robust, maximum width attained in anterior testic-
size. These discrepancies are curious and difficult to explain. There is ular field. Small tegumental spines anteriorly, diminishing posteriorly,
a great deal of overlap in meristic values between Looss' specimens absent posterior to acetabulum. Oral sucker subterminal, ovoid. Esoph-
and material collected from C. caretta in Shark Bay (Table I). Looss' agus sinuous, surrounded by glandular cells at cecal bifurcation. Intes-
specimens, as mentioned previously, appear to have been flattened se-tinal ceca bifurcate anterior to acetabulum, terminate near posterior end
verely during preparation. The range of measurements provided for H.of body. Acetabulum slightly pedunculate, ovoid, with minute spines
mistroides from the current study are somewhat smaller as they were on margin. Testes in preovarian, postovarian groups; individual testes
killed and fixed without mechanical flattening. difficult to differentiate. External seminal vesicle transversely elongate,
We petitioned the International Commission of Zoological Nomen- between preovarian testes and ovary. Cirrus sac well developed; cirrus
clature to exercise its plenary power to recognize H. loossi Price, 1934 spined, opening into a common genital atrium. Genital pore submedian,
as the type species of the genus (Platt and Blair, 1996; Case 2932) based sinistral; surrounded by sucker-like musculature without delimiting
on Art. 70b (misidentification of type species). Whereas Looss (1899) membrane forming true sucker. Ovary large, slightly lobed, between
did not describe a new species when erecting Hapalotrema, and his testicular groups. Oviductal seminal receptacle present, small; Laurer's
designation of H. constrictum was based on misidentification, no type canal not observed. Mehlis' gland not seen. Uterus small, passes anter-
specimen is currently recognized for this taxon. We, therefore, desig- iad and medially to enter genital atrium. Vitellarium granular, filling
nated specimen 2663 i 12 (left) (Alexandria vii.01) as the lectotype for extracecal space from posterior acetabular margin to cecal end, contin-
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PLATT AND BLAIR-REDESCRIPTION OF HAPALOTREMA SPP. 597
4 5
:...: ..... ,
FIGURE 4-5. 4. Ha
cirrus sac; e., egg
posterior group; v.
(scale bar = 250 pJ
ovary; t., anteriorm
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598 THE JOURNAL OF PARASITOLOGY, VOL. 84, NO. 3, JUNE 1998
TABLE II. Measurements of Hapalotrema synorchis Luhman, 1935 from the loggerhead turtle, Caretta caretta.
Vitellaria to:
and 9 mm X 2.1 mm; oral sucker and acetabulum 0.46 mm and 0.62
ovary slightly left of the midline of the body. The genital open-
mm in diameter, respectively; Takeuti [1942]) fall within the range of
ing shows muscular striations with a limiting membrane (Cribb
our specimens from C. caretta (Table II). The remaining features, sub-
median genital pore, genital pore approximately 30% of total length and Gordon, 1998). This is distinct from the genital musculature
from the posterior end of the body, and relative size of the oral sucker seen in H. synorchis. Laurer's canal arises from the oviduct near
and acetabulum, also fall within the range of H. synorchis. We consider the midline of the body, prior to the junction of the oviduct and
H. orientalis to be a junior synonym of H. synorchis.
vitelline duct, courses almost directly dorsad and is surrounded
by a raised muscular structure (see fig. 7 of Dailey et al.
DISCUSSION
[1993]). The meristic comparison of the 2 forms provided by
Cribb and Gordon (1998) presented new information on H. Cribb and Gordon (1998) reveals no significant differences. We
mehrai Rao, 1976 and considered H. dorsopora Dailey, Fast agree, therefore, that H. dorsopora should be regarded as a
and Balazs, 1993 a junior synonym. Dailey et al. (1993) de- junior synonym of H. mehrai.
scribed H. dorsopora from green turtles off the coast of Hawaii.The seminal receptacle is reported as either absent (Rao,
The new species was considered most similar to H. mehrai but 1976) or a separate saccate (Dailey et al., 1993) or canalicular
differed in its larger size, different disposition of the anterior (Cribb and Gordon, 1998) structure. We interpret the seminal
testes in the preovarian groups, anterior extent of vitellarium, receptacle to be an expansion of the oviduct from our exami-
and most importantly, the presence of separate male and female nation of the types of H. dorsopora, voucher material, and spec-
genital pores, with the female pore opening on the mid-dorsal imens in the junior author's collection. The same condition is
surface between the vitelline reservoir and the anteriormost tes- found in the 2 species of Hapalotrema redescribed above.
tes of the postovarian group. The female genital pore was sur- Mehrotra (1973) first proposed H. pambanensis as a new spe-
rounded by a raised sucker-like structure (Dailey et al., 1993). cies in an abstract that did not meet conditions for availability
Reexamination of the type material of H. dorsopora reveals a (Art. 13(a)(i); Anonymous, 1985) and is regarded as a nomen
typical arrangement of the reproductive system with the open- nudum. Gupta and Mehrotra (1981) subsequently described H.
ing of Laurer's canal misidentified as the female genital pore. pambanensis from the green turtle, hence the correct name and
We were unable to trace the oviduct from the ovary to the point authorship is H. pambanensis Gupta and Mehrotra, 1981, but
where it expands to form an oviductal seminal receptacle. From they failed to compare this species to H. mehrai. Specimens of
there the oviduct courses sinistrally and is joined by the duct both were collected from the same location in the same host
from the vitelline reservoir. The uterus turns sharply anteriad species from the same locale. Meristic comparison with H. meh-
and there is a partially collapsed egg in the uterus just under- rai (see Cribb and Gordon [1998]) revealed overlap in every
neath the junction of the left vitelline duct and the transverse character, and we agree that H. pambanensis should be consid-
vitelline duct. The uterus continues on to open, with the cirrus ered a junior synonym of H. mehrai.
sac, in the genital atrium located at the posterior edge of the Rao (1976) described H. postorchis as a new species in green
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PLATT AND BLAIR-REDESCRIPTION OF HAPALOTREMA SPP. 599
TABLE III. Reports of Hapalotrema spp. (Spirochidae) from marine turtles (Cheloniidae) from the coasts of Queensland (Qld.), Wester
(WA), and the Torres Straits, 1976-1993.
No. of
Host Parasite species Coll. no. Locality Year Location slides Accession no.*
Chelonia mydas Hapalotrema postorchis 1143 Badu Isl., Torres Straitt 1979 Artery near heart 1 QM G214162
1144 Badu Isl., Torres Strait 1979 Artery near heart 1 QM G214163
1145 Badu Isl., Torres Strait 1979 Artery near heart 1 QM G214164
1887 Townsville Harbor, Qld. 1993 Heart/liver 2 QM G214165
1890 Townsville Harbor, Qld. 1992 Various 10 QM G214166
Townsville Harbor, Qld.
Hapalotrema mehrai 1138 Magnetic. Isl., Qld. 1978 Heart 8 QM G214167
DB 1138
1139t Magnetic Isl., Qld. 1979 Heart 0 DB 1139
1140 Townsville Harbor, Qld. 1978 Heart 4 QM G214168
1141 Dalrymple Island, Qld. 1979 Heart 3 QM G214169
Dalrymple Island, Qld. DB 1141
1142 Townsville Harbor, Qld. 1979 Heart 1 QM G214170
DB 1142
1890 Townsville Harbor, Qld. 1992 Various 9 QM G214171
Hapalotrema sp. 1873 Townsville Harbor, Qld. 1992 Liver wash 3 QM G214172
1886 Townsville Harbor, Qld. 1992 Liver/lung wash 2 QM G214173
Caretta caretta Hapalotrema synorchis 1146t Shark Bay, WA 1979 Heart 0 DB 1146
1148 Shark Bay, WA 1979 Heart 2 QM G214174
DB 1148
Eretmochelys imbricata Hapalotrema mehrai? 1156 Magnetic Isl., Qld. 1978 Heart 1 QM G214182
1157 Magnetic Isl., Qld. 1978 Heart 4 QM G214183
turtles from the Gulf of Manar. While Rao (1976) reported find- We recognize 4 valid species of Hapalotrema Looss, 1899
ing numerous specimens of this fluke, he found only a single,that can be differentiated using the following key.
intact specimen to provide measurements for the description.
Dailey et al. (1993) provided a thorough redescription of H. Key to the species of Hapalotrema Looss, 1899
postorchis from Hawaii based on a wider range of material. Wela. Testes in anterior and posterior groups forming a compact mass,
have found this species in green turtles from various locations individual testes difficult to discern; genital sucker lacking
in the Coral Sea. limiting membrane ........... H. synorchis Luhman, 1935
An abbreviated list of marine turtles examined and Hapalo- (syn. H. orientalis)
lb. Testes discrete, not forming a compact mass ............. 2
trema spp. collected by the junior author during the past 22a. de-Total testes number >50 ............. H. mehrai Rao, 1976
cades is provided, along with information on the deposition of (syns. H. dorsopora, H. pambanensis)
voucher specimens in the Queensland Museum (Table III). Due 2b. Total testes number <30 ........................... 3
to the opportunistic nature surrounding the collection of much 3a. Genital pore located in anterior 1/2 of body ...... H. mistroides
(Monticelli, 1896) (syn. H. loossi)
of the material, meaningful estimates of prevalence and inten-
3b. Genital pore located in posterior /2 of body; genital sucker pres-
sity are not possible. All reports represent new locality records, ent, with limiting membrane ...... H. postorchis Rao, 1976
and H. mehrai from the hawksbill turtle (E. imbricata) is a new
host record. We feel that the information and specimens may ACKNOWLEDGMENTS
prove useful to other workers. Additional information on the
hosts and localities may be obtained from either of the authors T.R.P. was supported by a Lilly Open Fellowship during a
of the current work. sabbatical leave and thanks T Cribb (University of Queensland)
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600 THE JOURNAL OF PARASITOLOGY, VOL. 84, NO. 3, JUNE 1998
for a stimulating discussion of spirorchid anatomy. D.B. was imbricata (L.), from Puerto Rico. Proceedings of the Helmintho-
logical Society of Washington 43: 174-185.
supported by internal grants from James Cook University. J.
GUPTA, N. K., AND V. MEHROTRA. 1981. On two blood flukes (Trema-
Glazebrook and R. Lester assisted in the collection of blood toda) of the family Spirorchidae Stunkard, 1921 from Indian marine
flukes, and C. Limpus provided specimens from turtles exam- turtles. Acta Parasitologica Polonica 28: 11-20.
ined as part of other studies. Looss, A. 1899. Weitere Beitrage zur Kenntnis der Trematoden-Fauna
Aegyptens, zugleich Versuch einer natuirlichen Gleiderung des Ge-
nus Distomum Retzius. Zoological Jahrbucher (Jena) 12: 521-784
LITERATURE CITED LUHMAN, M. 1935. Two new trematodes from the loggerhead turtle (Ca-
retta caretta). Journal of Parasitology 21: 274-276.
ANONYMOUS. 1985. International code of zoological nomenclature. In- MEHROTRA, V. 1973. Digenea from some reptilian hosts in India, part
ternational Trust for Zoological Nomenclature, London, U.K., II. Proceedings of the Sixtieth Indian Science Congress, Part IV, p.
338 p. 46-47.
. 1997. Hapalotrema Looss, 1899 (Digenea): Hapalotrema loos- MONTICELLI, F S. 1896. Di un ematozoo della Thalassochelys caretta
si Price, 1934 designated as the type species. Bulletin of Zoological Linn. Internationale Monatsschrift fur Anatomie und Physiologie
Nomenclature 54: 190-191. 13: 141-172.
CABALLERO Y CABALLERO, E. 1962. Trematodos de las tortugas PLATT,deT. Mex-
R., AND D. BLAIR. 1996. Hapalotrema Looss, 1899 (Digenea):
ico. X. Presencia de Orchidasma amphiorchis (Braun, 1899) Looss, Proposed designation of H. loossi Price, 1934 as the type species.
1900 en una tortuga marina, Chelone mydas del las costas del es- Bulletin of Zoological Nomenclature 53: 1-3.
tado de Tamaulipas, Mexico. Anales de la Instituta de Biologia, PRICE, E. W. 1934. New genera and species of blood flukes from a
Mexico 33: 47-55. marine turtle, with a key to the genera of the family Spirorchidae.
Journal of the Washington Academy of Science 24: 132-141.
CRIBB, T. H., AND A. N. GORDON. 1998. Hapalotrema (Digenea: Spi-
RAO, S. L. 1976. On two new blood flukes (Trematoda, Spirorchidae)
rorchidae) in the green turtle (Chelonia mydas) in Australia. Journal
from the heart of Chelone mydas L. Acta Parasitologica Polonica
of Parasitology 84: 375-378. 24: 119-124.
DAILEY, M. D., M. L. FAST, AND G. H. BALAZS. 1993. Hapalotrema
SMITH, J. W. 1997. The blood flukes (Digenea: Sanguinicolidae and
dorsopora sp. n. (Trematoda: Spirorchidae) from the heart of the
Spirorchidae) of cold-blooded vertebrates: Part 2. Appendix I:
green turtle (Chelonia mydas) with a redescription of Hapalotrema Comprehensive parasite-host list; appendix II: Comprehensive
postorchis. Journal of the Helminthological Society of Washington host-parasite list. Helminthological Abstracts 66: 329-344.
60: 5-9. TAKEUTI, E. 1942. New blood-flukes of the family Spirorchidae from
FISCHTHAL, J. H., AND A. D. ACHOLONU. 1976. Some digenetic trema- Japanese fresh-water tortoise and marine turtles. Japanese Journal
todes from the Atlantic hawksbill turtle, Eretmochelys imbricata of Medical Science, Bacteriology and Parasitology 12: 161-174.
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