Hallinger MJ et al. (2020), Endoparasites infecting exotic captive amphibia...

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Parasitol Res 2020 Nov 01;11911:3659-3673. doi: 10.1007/s00436-020-06876-0.

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Endoparasites infecting exotic captive amphibian pet and zoo animals (Anura, Caudata) in Germany.

Hallinger MJ , Taubert A , Hermosilla C .

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Alongside exotic reptiles, amphibians, such as toads, frogs, salamanders, and newts, are nowadays considered popular pets worldwide. As reported for other exotic pet animals, amphibians are known to harbor numerous gastrointestinal parasites. Nonetheless, very little data are available on captive amphibian parasitic diseases. In this study, we applied direct saline fecal smears (DSFS) to examine in total 161 stool samples from 41 different amphibian species belonging to the orders Anura and Caudata. In addition, carbolfuchsin-smear (CFS) staining (n = 74 samples) was used to detect amphibian Cryptosporidium oocysts. Also, complete dissections of deceased amphibians (n = 107) were performed to specify parasite infections and to address parasite-associated pathogenicity. Overall, examined amphibian fecal samples contained 12 different parasite taxa. The order Rhabditida with the species Rhabdias spp. and Strongyloides spp. were the most prevalent nematode species (19.3%), followed by flagellated protozoans (8.7%), Amphibiocapillaria spp./Neocapillaria spp. (7.5%), Oswaldocruzia spp. (4.3%), Blastocystis spp. (3.1%), Cosmocerca spp. (3.1%), oxyurids (Pharyngonoidae) (3.1%), spirurids (1.2%), un-sporulated coccidian oocysts (0.6%), Tritrichomonas spp. (0.6%), Karotomorpha spp. (0.6%), and Cryptosporidium spp. (0.6%). One CFS-stained fecal sample (1.4%) was positive for Cryptosporidium oocysts. Within dissected amphibians, 31 (48.4%) of the anurans and 11 (26.2%) of the salamanders were infected with gastrointestinal parasites. One cutaneous Pseudocapillaroides xenopi infection was diagnosed in an adult African clawed frog (Xenopus laevis). Etiologically, 17 (15.9%) of them died due to severe parasitic and/or bacterial infections (e.g., Chryseobacterium indologenes, Citrobacter freudii, Sphingobacterium multivorum, Klebsiella pneumoniae). High prevalence and pathological findings of several clinical amphibian parasitoses call for more detailed investigation on gastrointestinal parasite-derived molecular mechanisms associated with detrimental lesions or even death.

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Genes referenced: pigy

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	Fig. 1 Selected pictures of helminth endoparasites. a Rhabdias sp.: adult nematodes inside the lung of a red-tailed knobby newt (Tylototriton kweichowensis). b Pseudocapillaria sp.: elongated nematode shed by red-eyed multicolored tree frog (Agalychnis callidryas). c Camallanus sp.: from a Spanish newt, Pleurodeles waltl. Please note the anterior buccal capsule armed with teeth. d Esophagus of Capillaria sp.: shed by an Eastern newt (Notophthalmus viridescens). e Free-living adult male of Rhabdias sp.: please notice posterior end mid gubernaculum, spirules, and cloaca (arrow)
	Fig. 2 Selected shed stages of endoparasitic nematodes. a Amphibiocapillaria sp./Neocapillaria sp.: brownish lemon-shaped eggs with two pole-clots. Shed by a crocodile newt (Tylototriton sp.). b Egg of Rhabdias sp.: shed by a Marañón Poison frog (Excidobates mysteriosus). c Oxyurid egg: bean-shaped, thick-walled eggs containing a morula. Shed by an Australian green tree frog (Litoria caerulea). d Amphibiocapillaria sp./Neocapillaria sp.: brownish lemon-shaped eggs with two pole-clots. Shed by a white-lipped horned toad (Megophrys major)
	Fig. 3 Histology of un-identified nematode infection in a smooth frog (Theloderma licin). a Notice adult nematode inside the intestinal lumen and diverse site-gated mucosal attached stages (arrows). b Enveloped intestinal larval stage: notice thick cuticula of the nematode (arrow)
	Fig. 4 Selected shed stages of protozoan endoparasites/commensals in amphibians. a Opalina sp.: heterokont from a yellow-bellied toad (Bombina variegata). Sparozoic Opalina lacking a mouth (cytostome) and covered with flagelliformic cilia. Inside are numerous similar nuclei. b Carbolfuchsin-stained fecal smear. Clearly detached are shed oocysts of Cryptosporidium sp. (arrows) by an Australian green tree frog (Litoria caerulea). These oocysts might come from prey animals, since captive Australian green tree frogs were fed with baby mice (Mutschmann, personal communication). c Vacular form of Blastocystis sp.: shed by Cranwells horned frog (Ceratophrys cranwelli). d Protoopalina sp.: heterokont form Hyperolius sp., Protoopalina sp., such as Opalina sp., seem to be most likely commensal, than parasitic. e Spores of Basidobolus sp.: Basidobolus is a filamentous fungus known to cause zygomycosis in amphibians, and shed spores can easily be mistaken for un-sporulated coccidian oocysts. f Trophozoites of Nyctotherus sp.: large trophozoites with lateral cytostomes and prominent macronuclei. Shed by red-eyed multicolored tree frog (Agalychnis callidryas)
	Table 1 Examined fecal samples of amphibians and origin of sender (total n = 161) regarding infection rate with endoparasites (%)
	Table 2 Performed necropsies of amphibians, order, and origin of sender (n = 107) regarding infection rate with endoparasites (%)

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