Captive Snake's Care As Parasite's Life Cycle Conservation Program

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Captive snake’s care In the literature digenean trematodes as parasite’s life cycle crawling in a snake’s oesophagus are casu- conservation program ally identified as Ochetosoma flukes (e.g. SCHNELLER & PANTCHEV 2008), although this genus is definitely a member of the Formidable parasitic infections are a neotropic realm and, in cases of recurring common health problem in exotic reptiles infestations of pet snakes in Europe, this lately introduced to European pet markets. exotic distome would thereby be designated Besides the common acts of negligence, an exceptional neozoon, as it would be an some immanent noxious effects during ac- invasive animal in an artificial ecosystem. climatization may aggravate the wasting of The visual nature of the parasites detected is the reptile, especially stress by enforced en- however perfectly consistent with the mor- closure, lack of hygiene, and many a well- phological description of the Palearctic anu- intentioned animal keeper’s erratic behav- ran fluke genus Pleurogenoides (TRAVAS- ior. Merging into biological oddities like SOS, 1921; Trematoda: Lecithodendriidae) progenesis, that is premature sexual matura- according to RYZHIKOV et al. 1980. In tion in a morphologically juvenile organ- Europe, the distribution area of the genus ism, peculiar epidemiological effects con- Pleurogenoides presumably covers the cerning the intermediate hosts (= the organ- range area of its key host, water frogs of the isms in which a parasite passes its larval, genus Rana, keeping in mind the unsettled pre-sexual existence) and the definitive host species differentiation within this genus. (= the organism in which a parasite gains its The fluke’s body (Fig. 2) is elliptical, with adult and sexual existence) of parasites may rounded anterior and posterior ends, up to result. This case report is given to expert 2.0 mm in length, 0.56 mm in maximum keepers of exotic animals and pets, her- width at the level of testes; the surface is petologists and reptile veterinarians with the armed with dense spines at the anterior end, intention to evoke thoughtfulness on the which disappear toward the posterior end of unanticipated effects, while creating the the body. The oral sucker is sub-terminal artificial biocenosis. and spherical, the ventral sucker lays almost A Bristly Bush Viper Atheris hispida equatorial and is slightly smaller than the LAURENT, 1955, recently imported from oral one. The uterus is located post-acetabu- Uganda via Slovakia to Austria, weighing lar and post-testicular, it occupies the entire 24 g, died briskly five weeks after being area up to the hind region of the body, and it force fed on reportedly defrosted autochtho- forms numerous ascending and descending nous water frogs (Rana sp.) with symptoms coils. It is filled with many ovoid, dark of a disseminating Monocercomonas infec- brown eggs of 0.03 mm x 0.016 mm; and tion (RICHTER et al. 2008). Necropsy re- these egg-filled uteri are distinguishable as vealed cachexia, severe anaemia, and an in- brown spots even in Fig. 1. festation with about three hundred opaque, The obligatory parasitic trematode exsanguinous flukes adhered to the mucosa Pleurogenoides has been considered to pass of the oral cavity (Fig. 1), oesophagus and through a straightforward, indirect repro- stomach. The eye-catching, but obviously duction cycle, including two intermediate minor pathogenic distomes were identified hosts, freshwater snails (Lymnea, Bithynia, as Pleurogenoides sp., most probably P. me- Planorbarius) and dragonfly larvae, and dians (OLSSON, 1876) or P. compactus European anurans, Rana, Hyla, Bufo, Bom- (STROM, 1940), by morphological and bio- bina, and Pelobates, as definitive host (e.g. metrical criteria after the implementation of BESPROZVANNYKH 2000; DÜŞEN & ÖZ 2004; a carmine staining (ODENING 1955; AND- ANDREAS 2006). Surprisingly, apparently REAS 2006). Additionally, an infection with grown-up flukes of Pleurogenoides tener the facultative pathogenic protozoan Mono- (LOOSS, 1898) were detected naturally para- cercomonas sp. was diagnosed by gene sitizing Egyptian chameleons (Chamaeleo amplification, mainly in the cloaca, ureters, chamaeleon LINNAEUS, 1758) (GROSCHAFT & kidneys and the pancreas (RICHTER et al. MORAVEC 1983) and Ukrainian Sand Lizards 2008). (Lacerta agilis LINNAEUS, 1758) (MACY All_Short_Notes.qxd 06.08.2010 15:08 Seite 6

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84 SHORT NOTE HERPETOZOA 23 (1/2) Wien, 30. Juli 2010 SHORT NOTE

Fig. 1: Pleurogenoides sp. in the oral cavity Fig. 2: Pleurogenoides sp., dorsal view, of Atheris hispida LAURENT, 1955. carmine staining, bar: 0.4 mm.

1964) even – observations, which generate penetrate the tissue of the ingested frog cor- the problem of the genuine host status of the pus, and adhere to the oesophagus of the taxons subjected to infection. In considera- predator for an ultimate chance of egg depo- tion of the known facultative progenesis of sition. This option of some distomes, but this distome (GRABDA KAZUBSKA 1976; LE- definitely not P. medians, was experimental- FEBVRE & POULIN 2005), an alternative inter- ly verified some years ago, regrettably writ- pretation of the observations can be given: ten down as a non citable reference (BOZH- dragonfly larvae act as paratenic hosts (= a KOV without year). Fourthly, and the hypo- substitute of an intermediate host, in which thesis with maximum parsimony, Pleuro- no ontogenetic development of the parasite genoides is an exceptional fluke genus modi- occurs), and a modified life cycle involving fying its life-cycle according to ecological precocious metacercaria becomes operative requirements, integrating paratenic hosts and immediately. Our case report may spotlight skipping definitive or intermediate hosts this topic – four hypotheses of ascending (GRABDA KAZUBSKA 1976). As the metacer- probability are addressed: caria of P. medians attain such a degree of First, in Central Africa exists a yet un- maturity that they do not only produce viable described, Pleurogenoides-like Ochetosoma eggs, but cannot be distinguished from gen- species with an unknown life cycle and Bush uine adults morphologically (= neoteny; Vipers as the definitive host. Secondly, Pleu- LEFEBVRE & POULIN 2005), the second inter- rogenoides is a bizarre parasite genus, in mediate host, water frogs, may occasionally Europe able to use anurans as genuine defin- be considered as the definitive host – making itive hosts where anurans are common, and Pleurogenoides a classic anuran parasite. Squamata elsewhere. Thirdly, the adult dis- The European Pleurogenoides flukes seem tomes may survive the gorging of their hosts, to display facultative life-cycle modifica- All_Short_Notes.qxd 06.08.2010 15:08 Seite 7

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tions as alternative survival strategies, with toriya; Sofia. DÜŞEN, S. & ÖZ, M. (2004): Helminth pa- normal, modified, and abbreviated cycles rasites of the Tree Frog, Hyla arborea (Anura: Hylidae) from Southwest Turkey.- Comparative Parasitology, simultaneously present in the parasite popu- Lawrence; 71 (2): 258-261. GRABDA KAZUBSKA, B. lations. The evolutionary force behind this (1976): Abbreviation of the life-cycles in plagiorchid oddity is the infrequency of the transmission trematodes: general remarks.- Acta Parasitologica Polo- act between intermediate and definitive host. nica, Warsaw; 24: 125-141. GROSCHAFT, J. & MORA- VEC, F. (1983): Some trematodes and cestodes from The metacercaria of Pleurogenoides infect amphibians and reptiles in Egypt.- Vestnik Ceskoslo- an intermediate host, perennial water frogs, venské Spolecnosti Zoologické, Praha; 47: 241–249. that outlive the parasite (LAGRUE & POULIN LAGRUE, C. & POULIN, R. (2009): Life-cycle abbrevia- 2009). A fortuitous transmission of the pre- tion in trematode parasites and the developmental time hypothesis: is the clock ticking?- Journal of Evolution- cocious parasite larva to the genuine defini- ary Biology, Penryn; 22 (8): 1727-1738. LEFEBVRE, F. tive host puts the life-cycle simply back on & POULIN, R. (2005): Progenesis in digenean trema- track – as observed in the case presented. todes: a taxonomic and synthetic overview of species Especially stenoecious and thus fre- reproducing in their second intermediate hosts.- Para- sitology, Cambridge; 130 (6): 587-605. MACY, R. W. quently endangered exotic reptile species (1964): Life-cycle of the digenetic trematode Pleuro- seem to be favored victims of grotesque genoides tener (LOOSS, 1898) (Lecithodendriidae).- parasitism caused by bizarre, opportunistic Journal of Parasitology, Lawrence; 50: 564-568. and/or facultative pathogenic microorgan- ODENING, K. (1955): Die Zooparasiten der Frösche Deutschlands.- Wissenschaftliche Zeitschrift der Fried- isms in captivity. Even well meant actions rich-Schiller-Universität Jena, Jena; 3 (3/4): 179-215. of the reptile keeper can produce counter- RICHTER, B. & HASSL, A. & KÜBBER-HEISS, A. (2008): productive effects, if an infective organism Akzidentelle Infestation von Rauschuppen-Busch- with an unknown ecology establishes itself vipern (Atheris hispida) mit einer heimischen Tremato- denart?- Deutsche Tierärztliche Wochenschrift, Han- in the artificial ecosystem of captive reptile nover; 115 (9): 349-350. RYZHIKOV, K. M.& SHARPILO, care. In the case described, the only signifi- V. P. & S HEVECHENKO, N. N. (1980): Helminths of am- cant noxious effect detected during trans- phibians of the fauna of the USSR; Moskva port and acclimatisation of the snake was (Izdatel’stvo Nauka), 278 pp. SCHNELLER, P. & PANT- CHEV, N. (2008): Parasitologie bei Schlangen, Echsen the feeding with local frogs, apparently und Schildkröten. Ein Handbuch für die Reptilienhal- housing autochthonous parasites, which tung; Frankfurt/Main (Edition Chimaira) [Frankfurter could not be killed by short-time freezing in Beiträge zur Naturkunde, vol. 40], 205 pp. a domestic refrigerator. Establishing breed- AUTHORS: Andreas R. HASSL, Micro-Biology ing in captivity of rare and endangered rep- Consult Dr. Andreas Hassl, Ameisgasse 63-4-12, 1140 Vienna, Austria; Barbara RICHTER & Anna KÜBBER- tiles simultaneously broadens the life basis HEISS, Institute of Pathology and Forensic Veterinary of some odd parasitic organisms – undesir- Medicine; Department of Pathobiology; University of able, but unavoidable effects, which confer Veterinary Medicine Vienna; Veterinärplatz 1, 1210 species conservation efforts an extensive, Vienna; Austria extraordinary, and maybe even innovative subject matter. ACKNOWLEDGMENTS: The authors grate- fully acknowledge the supportive cooperation of Walter HIRSCHMANN (Vienna). KEY WORDS: Reptilia: Squamata: Serpentes, Atheris hispida, Bristly Bush Viper; Trematoda, Di- genea, Pleurogenoides medians, Pleurogenoides compactus, trematode infection, fluke, anura, Rana, progenesis, definitive host, parasitology, exotic pet keeping SUBMITTED: June 18, 2009 REFERENCES: ANDREAS, K. (2006): Helmin- then einheimischer Froschlurche. Inaugural–Dissertati- on, Freie Universität Berlin; Berlin; 123 pp. BESPROZ- VANNYKH, V. V. (2000): The biology of the trematodes Nenimandijea kashmirensis and Pleurogenoides medians (Pleurogenidae) - parasites of frogs in the Maritime Territory.- Parazitologiia, Sankt-Peterburg; 34 (4): 349- 354. BOZHKOV, D. (without year): Experimental inves- tigation into the passage of mature helminths from the body of ingested frogs into the body of a water snake.- Izvestiya na Tsentralnata Khelmintologichna Labora-