Original Papers Preliminary Coproscopic Examination of Tortoises in the City Zoological Garden in Wroclaw, Poland
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Wiadomoœci Parazytologiczne 2011, 57(4), 249–251 Copyright© 2011 Polish Parasitological Society Original papers Preliminary coproscopic examination of tortoises in the City Zoological Garden in Wroclaw, Poland Katarzyna Buńkowska, Anna Okulewicz, Agnieszka Perec-Matysiak, Joanna Hildebrand Department of Parasitology, Institute of Genetics and Microbiology, Wroclaw University, 63/77 Przybyszewskiego Street, 51-148 Wroclaw, Poland Corresponding author: Anna Okulewicz; E-mail: [email protected] ABSTRACT. Tortoises are a novelty in the world of pets. Although a great deal of information has been acquired on the internal medicine and surgery on these animals, little is known of their parasitological fauna. Fecal samples of 11 species of tortoises housed in the City Zoological Garden in Wroclaw were examined. Eggs of parasitic helminths were isolated using flotation and sedimentation techniques. The overall prevalence was 81.2%. Two groups (Nematoda and Trematoda) of endoparasites were found. Oxyurid eggs were found almost in every animal examined. Co-infection with oxyurids and ascarids was recorded for T. horsfieldii and T. marginata . Three species of tortoises were infected by digenic trematodes. Key words: tortoises, helminths, coprological examination, zoo garden Introduction other reptiles are plagued with. It is little known about most parasites of these animals and, for many, The order Chelonia contains a group of animals we have no idea whether the parasites are pathogens that evolved into a shelled form millions of years or benigns (commensals). However, there are ago and is considered the most primitive group of several parasites that can cause severe problems, if living reptiles. Chelonians include turtles, tortoises they are not properly treated. Most parasitic and terrapins and these terms have different problems occur when reptiles are either kept in close meanings in different parts of the world. In the captivity with other animals or when kept in United States, tortoises refer to terrestrial animals, unsanitary conditions (e.g. dirty water, without turtles usually to aquatic or semiaquatic and proper protection against insects). terrapins – to semiaquatic, hard-shelled chelonians. The aim of this study was to determine the These animals are becoming very popular as pets occurrence of intestinal helminths from tortoises especially in Europe where there is a long history of housed in the City Zoological Garden in Wroclaw. keeping the Mediterranean Testudo species as garden pets. Although the report from the CDC [1] Material and methods discourages the adoption of tortoises as pets, the appearance of this „living fossil” has favored the The coprological examination was carried out on change of its role in the modern human society from 11 species of chelonians: Hermann’s Tortoise an „ornamental” garden animal to a unconventional (Testudo hermanni ), Horsfield’s Tortoise ( Testudo pet living inside our houses [2]. According to Rivera horsfieldii ), Marginated Tortoise ( Testudo margina - [3] there are hundreds of species of chelonians kept ta ), Leopard Tortoise ( Stigmochelys pardalis ), in captivity. Asian Forest Tortoise ( Manouria emys ), Bell’s Chelonians are not susceptible to as many Hinged Tortoise ( Kinixys belliana ), Elongated varieties of parasites as most mammals, birds and Tortoise ( Indotestudo elongata ), Radiated Tortoise 250 K. Buñkowska et al. Table 1. General information on the tortoises species examined and their parasites Parasites Host species Origin Diet D igenea Nematoda Pharyngodonidae Ascarididae Astrochelys r adiata Madagascar herbivores + + – Chelonoides nigra Galapagos Islands herbivores – + – Geochelone elegans India and Sri Lanka herbivores – + – Geochelone sulcata Africa herbivores – + – Indotestudo elongata Asia basically herbivores – + – Kinixys belliana Africa omnivores + – – Manouria emys Asia omnivores + – – Stigmochelys pardalis Africa herbivores – + – Testudo hermanni Europe herbivores – – – Testudo horsfieldii Asia herbivores – + + Testudo morginata Europe herbivores – + + (Astrochelys radiata ), Galapagos Giant Tortoise noticed the occurrence of these parasites in 10 (Chelonoidis nigra ), Indian Star Tortoise ( Geoche - species of chelonians, most frequently in Hermann’s lo ne elegans ), and African Spurred Tortoise Tortoises (92.5%). In our own research the eggs of (Geochelone sulcata ). That last species deserves oxyurids were identified only to the family level, special attention because it is rarely encountered in because eggs of pinworms affecting tortoises zoological gardens and there is only one individual retrieved at the coprological examination are in Poland in the Wroclaw ZOO. Details about the impossible to identify to species and genus level. diet of host species and their origin are presented in Existing data on this nematode group mainly deal Table 1. with taxonomy and morphological descriptions of The faeces of reptiles were macroscopically adult specimens spontaneously eliminated by the examined for the presence of adult parasites. For the reptiles or retrieved post-mortem [8–12]. According eggs presence of intestinal helminths, individual to the above-mentioned articles the following stool samples were examined by routine flotation oxyurid genera occur in tortoises: Tachygonetria , and sedimentation methods. During flotation Mehdiella , Thaparia and Alaeuris . Tachygonetria procedure a saturated NaCl solution with a specific spp. nematodes found in tortoises exhibit a wide gravity of 1.2 was used, whereas sedimentation geographical distribution, with five species and four method was performed using tap water. subspecies from the Ethiopian region (Madagascar Identification of eggs was conducted under the light and South Africa), nine Palaearctic species and four microscope. subspecies, two species from the Nearctic region (Mexico) and one species from the Neotropical Results and discussion region (Galapagos Islands). This genus occurs in all major biogeographical regions with the exception of As shown by the preliminary coproscopical the Australian region [10]. The majority of survey, the overall prevalence of endoparasites in pharyngonid species of Palearctic tortoises, such as tortoises was 81.2%. The most frequent parasites T. hors fiel dii , T. her man ni , are mem bers of this ge - were oxyurids of the Pharyngodonidae family. nus, whi le pha ryn go nid spe cies from Ne arc tic tor to - According to the literature, oxyurid infection is ises in ter alia Go phe rus agas si zii are mem bers of common among chelonians, especially herbivorous Ala eu ris [8]. The re is no in di ca tion on the oxy urid species [2,4–6]. This may be explained mainly by fau na from Orien tal tor to ises (e.g. G. ele gans , their low pathogenicity, their ability to survive I. elon ga ta and M. emys ), from Cen tral and West hibernation [7], by the monoxenous life cycles of Afri ca ( K. bel lia na, K. ero sa, G. sul ca ta ) and from these parasites and the behavior and ecology of their Neotropical tortoises [10]. hosts. We confirmed eggs occurrence of these Co-infection of oxyurids and Angusticaecum parasites in 8 different host species. Rataj et al. [6] holopterum were noted in each individual of Preliminary coproscopic 251 T. horsfieldii and T. marginata . A. holopterum has eterinaria Scandinavica 53: 33. been reported twice in Poland in Trachemys scripta [7] Capelli G., Borsato E., Stancampiano L., Bozzolan elegans obtained from Wroclaw pet shop [13] and G., Pietrobelli M. 1998. Epidemiology of gastro - from Poznan Zoological Garden [14]. The presence intestinal parasites of tortoises ( Testudo hermanni of this parasite has also been recorded in Italy in boettgeri ) in captivity. Parassitologia 40: 29. [8] Bouamer S., Morand S., Bourgat R. 2001. Oxyuroids Testudo graeca [4]. of Palaearctic Testudinidae-new definition for In our investigation Trematoda eggs were found Alaeuris Seurat, 1918 (Nematoda: Pharyngodonidae) in omnivorous tortoises ( M. emys and K. belliana) and redescription of Alaeuris numidica (Seurat, and in one herbivorous individual of A. radiata , 1918). Journal of Parasitology 87: 128-133. which was kept on the grassy outdoor area with [9] Bouamer S., Morand S., Bourgat R. 2001. other omnivorous chelonians. The high prevalence Redescription of Mehdiella microstoma and of Trematoda were found in Marginated Tortoises – description of Mehdiella petterae sp. n., with a new 60% and Spur-thighed Tortoises – 26.4% from definition of the genus Mehdiella Seurat, 1918 Lebanon and Slovenia [6]. (Nematoda: Pharyngodonidae). Folia Parasitologica It is worth to notice that tortoises in the City 48: 132-138. [10] Bouamer S., Morand S. 2002. Description of Zoological Garden in Wroclaw receive constant Tachygonetria combesi n. sp. and redescriptions of care of veterinarians. The high prevalence of four species of Tachygonetria Wedl, 1862 helminths in examined chelonians indicates that (Nematoda: Pharyngodonidae), with a new diagnosis parasites of these animals are difficult to eradicate. of the genus . Systematic Parasitology 53: 121-139. [11] Bouamer S., Morand S. 2003. Descriptions of two References new species of the genus Tachygonetria Wedl, 1862 (Nematoda–Pharyngodonidae) and discussion of the [1] CDC. 2003. Reptile-associated salmonellosis – relationships among the species of the genus. Parasitology Research 91: 68-73. selected states, 1998–2002. Morbidity and Mortality [12] Bouamer S., Morand S. 2003. Phylogeny of 52: 1206-1209. Palaearctic Pharyngodonidae