The intestinal parasites of the selected mammal species, living in zoological gardens and wild animal parks



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Roczniki Naukowe Polskiego Towarzystwa Zootechnicznego, t. 6 (2010), nr 3 The intestinal parasites of the selected mammal species, living in zoological gardens and wild animal parks Justyna Bartosik 1, Paweł Górski 2 Warsaw University of Life Sciences (SGGW); 1 Faculty of Animal Sciences, Department of Animal Breeding, Unit of Pig Breeding, 2 Faculty of Veterinary Medicine, Department of Pre-clinical Sciences, Unit of Parasitology and Invasiology; Ciszewskiego 8, 02-786 Warsaw Parasite infections are still one of the main reasons for veterinary problems in zoological gardens. In our investigations, we aimed at updating our knowledge about internal parasite infections of mammals kept in captivity in Poland. From November 2006 to June 2007, 274 fecal samples from 53 mammal species were collected and then, examined, using standard flotation and sedimentation techniques. The investigated animals were kept in Warsaw, Łódź and Płock zoological gardens, and also in Park of Wild Animals in Kadzidłowo. In total, 9 species of roundworms (Nematoda) and 3 species of protozoans from Eimeria genus have been detected. The most common parasites have been found: gastro intestinal nematodes from and Molineidae family. The incidence of all parasitic invasions in the examined animals from zoos was equal to 20-28% whereas in the Park of Wild Animals in Kadzidlowo it was considerably higher (48%). Baylisascaris transfuga, the eggs of which have been found in faecal samples of polar bear, is a species which may be dangerous for human health. Key words: intestinal parasites / zoological garden Parasite infection of animals, living in zoological gardens and wild animal parks are nowadays still a serious veterinary problem. This is one of the reasons for losses of valuable animal species [1, 10]. There is a risk that new parasite species will be brought into zoos area. The important role in parasites spreading out is played by wild birds and free- -living mammals. They have better living condition in zoological gardens (an access to food, warm places to hide during the winter season, etc.). Unfortunately, they can be also a reservoir of many parasitic diseases [18]. In many cases, the wild animals such as birds, martens, cats, rodents and invertebrates may be the additional parasitic invasion source (as intermediate host or vectors of parasites) [7, 12]. The exotic animals which have been kept in Polish climate condition for many generations assimilate our parasitic fauna that does 143

not occur in their natural environment [17]. On the other hand, the animals imported from different countries to Polish zoos may possess new parasite species [6, 19]. The earlier experiments, conducted in Belgium have shown that the type of animal paddock plays an important role in development of parasite invasion. The sandy and grassy paddock may be a reservoir of parasite forms [3, 7, 8]. That is why it is important to keep the adequate zoohygienical standards, the animals faeces should be removed every day away. Moreover, a particular care should be taken of employees, working with the infected animals, which may be carrier of parasite species, being also dangerous for other animals and human health [13, 15]. An Echinococcus granulosus, the cosmopolitan cestode, the larvae of which affect many mammal organs (especially liver) of the animals who are kept in the zoos is one of the discussed species. A man may be incidental intermediate host of this parasite. The disease may be dangerous, especially when hydatid cysts are situated in the brain, acute encephalitis may be fatal [5]. Therefore, it is necessary to study the pathogenicity of parasites, to keep control and apply deworming medicines to prevent, or to limit the spreading of invasion. The main aim of the present research was to indentify the species composition of parasitic fauna, characteristic of the mammals kept in zoological gardens and wild animal parks. Material and methods The research material derived from 3 zoological gardens (Warsaw, Łódź and Płock) and from Wild Animal Park in Kadzidłowo. From November 2006 to June 2007 the fecal samples, which were collected from 53 mammals have been twice examined: in the autumn-winter season and summer-spring seasons. Standards coproscopy methods have been used (flotation and sedimentation). In total, 274 fecal samples have been examined, 64 came from Warsaw ZOO, 60 from Płock ZOO, 46 from Łódź ZOO and 104 from Kadzidłowo Park. The eggs and oocysts, which have been found in the material were photographed, using Panasonic GP camera with LUCII computer program and then, diagnosed. In this research NICON ECLIPSE TE200 and OLIMPUS CX21 microscopes have been used. Results and discussion In fecal samples from the mammals, living in Warsaw ZOO, 4 parasite species belonging to Nematoda phylum (one being not determined) and 1 species belonging to Apicomplexa phylum, were found. In the material collected in the Łódź ZOO, invasion of 5 species from Nematoda (two species were specified, the remaining ones were only determined on the level of family or not identified at all) and one species of coccidia (specified as representative of Eimeria family) were recorded. In the samples collected from Płock ZOO, 7 species, were found, which belonged to Nematoda phylum (one indentified on the level of family and one being not identified). In material coming from Kadzidłowo, the eggs of 9 parasite species, also belonging to Nematoda phylum have been recorded (4 of them were identified on the level of genus and 5 of them on the level of family). Moreover, 2 Protista species were detected. 144

Fig. Extensiveness of parasite infections in four different places Rys. Ekstensywność inwazji pasożytniczych w czterech badanych ośrodkach hodowlanych In total, 9 species of Nematoda phylum and 4 species of Apicomplexa phylum were identified. In some cases, it was difficult to establish systematic position of parasites ( family). The eggs within the mentioned family are often not easily distinguished. The prevalence of parasite infections in mammals kept in zoological gardens was found on similar level (22-28%); it was higher in Kadzidłowo (ca. 48%) (Fig.).The results of fecal samples from mammals living in zoological gardens and wild animal parks are given in the Table. The results of the studies in autumn-winter period are different than those ones, obtained in the spring-summer season. In the second stage of the studies, there were found the parasite eggs which were not recorded in the first period of the experiment and vice versa (few cases). The percentage of the infected animals (in relation to all the examined species) in the particular centres is illustrated in the figure. The most common parasite species occurred in the material, belonging to Nematoda phylum. The other authors suggested that the reason for this situation was caused by a simple life cycle of this parasite species [16, 17, 21]. Moreover, a high concentration of animals on paddocks may affect easy spreading out of invasion; it causes a considerable concentration of larvae or invading eggs on a small area [2]. Relatively high temperature and humidity of housing for animals are favourable for growth and development of parasite eggs and larvae. The sandy and grassy paddock may be a source of many roundworms at different stages; the wild birds and rats may bring them into the cages [4, 18]. Surprising, any invasion of parasite species belonging to Trematoda and Cestoda class has not been detected, probably due to their complicated larval development what is often impossible or very difficult in the zoological gardens conditions because of the lack of intermediate hosts. 145

Table Tabela Results of faeces examination from three zoological gardens (ZOO) and from Park of Wild Animals in Kadzidłowo Zestawienie wyników badań kału zwierząt pochodzących z trzech ogrodów zoologicznych i Parku Dzikich Zwierząt w Kadzidłowie parasite species gatunek pasożyta Autumn-winter season Sezon jesienno-zimowy host species gatunek żywiciela parasite species gatunek pasożyta Spring-summer season Sezon wiosenno-letni host species gatunek żywiciela 1 2 3 4 ZOO Warsaw ZOO Warszawa Isospora felis serval serwal Isospora felis serval serwal Toxascaris leonina lion lew, snow-leopard irbis (pantera śnieżna) Toxascaris leonina lion lew, snow-leopard irbis (pantera śnieżna) Trichuris vulpis African wild dog likaon Trichuris vulpis African wild dog likaon Baylisascaris transfuga n.n. Polar bear niedźwiedź polarny South american coati ostronos not examined (death of animal) nie badano (śmierć zwierzęcia) ZOO Płock Toxocara cati, Toxascaris leonina snow-leopard irbis (pantera śnieżna) Toxocara cati, Toxascaris leonina snow-leopard irbis (pantera śnieżna) Trichuris trichiura Lar gibbon gibbon białoręki, Patas-monkey koczkodan rudy Trichostrongylus axei donkey osioł domowy, pony kuc n.n. South american coati ostronos n.n. Red kangaroo kangur rudy Roundworms from Ilama lama 146

1 2 3 4 ZOO Łódź Eimeria sp. Asian elephant słoń indyjski Roundworms from Asian elephant słoń indyjski Parascaris equorum plains zebra zebra stepowa n.n. tapir Toxocara sp. Nine-banded Armadillo pancernik peba Trichostrongylus axei donkey osioł domowy Wild Animal Park in Kadzidlowo Park Dzikich Zwierząt w Kadzidłowie Strongyloides papillosus moose łoś Trichuris ovis moose łoś Eimeria nina-kohl-yakimovi mouflon muflon Eimeria faurei mouflon muflon Roundworms from Nematodirus sp. mouflon muflon, deer jeleń, moose łoś Roundworms from Roundworms from mouflon muflon, mountain hare zając bielak, chamois kozica, deer jeleń, roe deer sarna, reindeer renifer mouflon muflon American bison bizon, deer jeleń, moose łoś Trichostrongylus axei Przewalski s horse koń Przewalskiego n.n. European otter wydra europejska n.n. European polecat tchórz zwyczajny n.n. indeterminate Nematoda eggs nieoznaczone jaja nicieni no parasitic invasion nie stwierdzono inwazji pasożytniczej 147

When evaluating the results of own studies, we considered the occurrence of periodical fluctuations in production of eggs of a given parasite; it is also important to take into consideration the fact of the temporary fluctuations of parasite eggs production and prepatention period since the time of the penetration of host s body by the parasite until his maturation. The coproscopy studies, performed during the discussed period give always negative results [18, 19]. In the Park of Wild Animals in Kadzidłowo where the living conditions of the animals are most similar to natural environment, the representatives of roundworms, belonging to constitute the most numerous group of the indentified parasites. The invasion of the mentioned parasites has the greatest meaning, from medical point of view, for ruminants. It concerns also deer, roe-deer and fallow deer population kept, in captivity [15] as well as mammals living in zoological gardens [3]. The periodical larval hypobiosis is a phenomenon, characteristic of the parasite species belonging to, therefore the results of fecal samples examination from autumn-winter season were negative [4]. On the other hand, in the same material collected from the spring-summer season, probably thanks to the spring rise phenomenon, the parasite eggs were found. The intensity and extensiveness of the level of invasion could be also caused by deworming preparations. In the discussed zoological gardens and in Wild Animals Park deworming was carried out with the application of various pharmaceutical products. The highest level of invasion in animals living in Kadzidłowo could result from a natural character of paddocks and contacts with animals and their faeces what was reported by the employees of the Park. The evaluated and analyzed material did not contain any eggs of parasites which are found in the animals, living in the closed units outside the borders of Poland. In the own studies, the species belonging to Nematoda and Apicomplexa phylum were most frequently found in many mammal species. They include the species from Toxocara type, dog and cat worms from Trichuris type or coccidia from Eimeria. In fecal samples from polar bear, Baylisascaris transfuga eggs were found. The mentioned parasite species is rare in domesticated animals and may be dangerous for humans [9]. Establishment of species composition of parasites in the mammals, living in the zoos is possible when the research work is conducted with abundant animal material and when the test includes faeces, blood and urine. The application of modern techniques and diagnostic methods (PCR, immunological tests e.g. ELISA) and animal cross-section constitutes the basis for complete and reliable evaluation of parasitological situation [20]. The conducted studies were treated as preliminary ones, having a screening character. They allowed assessing the level of invasion intestinal parasites in the animals, living in the zoological gardens of central Poland. REFERENCES 1. ASANO R., MURASUGI E., YAMAMOTO Y., 1997 Detection of intestinal parasites from main-land raccoon dogs, Nyctereutes procyonoides viverrinus, in southeastern Kanagawa Prefecture. The Journal of the Japanase Associasion for Infection Diseases 71, 664-667. 2. GARIJO M.M., ORITZ J.M., RUZI DE IBANEZ M.R., 2004 Helminths in giraffe (Giraffa camelopardalis girafa) from a zoo in Spain. Onderstepoort Journal of Veterinary Research 71, 153-156. 148

3. GOOSSENS E., DORNY P., BOOMKER J.,VERCAMMEN F., VERCRUYSSE J., 2005 A 12-month survey of the gastro-intestinal helminths of antelopes, gazelles and giraffids kept at two zoos in Belgium. Veterinary Parasitology 127, 303-312. 4. GUNDŁACH J.L., SADZIKOWSKI A.B., 2004 Parazytologia i parazytozy zwierząt. PWRiL, Warszawa. 5. KADŁUBOWSKI R., 1999 Zarys parazytologii lekarskiej. PZWL, Warszawa. 6. KOTECKI N., 1970 Circulation of the cestoda fauna of Anseriformes in the Munticipal Zoological Garden in Warsaw. Acta Parasitologica 17, 329-355. 7. KRYNICKA I., RZECZKOWSKA M., ZŁOTORZYCKA J., 1979 Zarobaczenie małp człekokształtnych i zwierzokształtnych we wrocławskim ogrodzie zoologicznym. Wiadomości Parazytologiczne 25, 655-664. 8. OKULEWICZ A., Kruczkowska B., 1988 Pasożyty jelitowe małp wrocławskiego ZOO. Wiadomości Parazytologiczne 34, 301-305. 9. PAPINI R., RENZONI G., PICCOLO S., L.,O., CASAROSE L., 1996 Ocular larva migrant and histopathological lesions in mice experimentally infected with Baylisascaris transfuga embryonated eggs. Veterinary Parasitology 61, 315-320. 10. POCIELNIK O., 1973 Pasożyty jelitowe małp z ogrodu zoologicznego we Wrocławiu. Wiadomości Parazytologiczne 23, 289-296. 11. SATO C., KAWASE S., YANO S., NAGANO H., FUJIMOTO S., KOBAYASHI N., MIYA- HARA K., YAMADA K., SATO M., KOBAYASHI Y., 2005 Outbreak of larval Echinococcus multilocularis infection in Japanese monkey (Macaca fuscata) in a zoo, hokkaido: Western blotting patterns in the infected monkeys. Journal of Veterinary Medicine Science 67 (1), 133-135. 12. SATO H., UNE Y., TAKADA M., 2005 High incidence of the gullet worm, Gongylonema pulchrum, in a squirrel monkey colony in a zoological garden in Japan. Veterinary Parasitology 127, 137-137. 13. SHU-YI Z.,U., MEI-XIONG W., ZHONG-YONG Z., JIAN-YI Y., XIN-QUAN S., 2000 Prevalence of antibodies to Toxoplasma gondii in the sera of rare wildlife in the Shanghai Zoological Garden, People s Republic of China. Parasitology International 49, 171-174. 14. STEFAŃSKI W., 1968 Parazytologia weterynaryjna. PWRiL, Warszawa. 15. TROPIŁO J., KISZCZAK L., KRYŃSKI A., 1999 Łowiectwo (weterynaria i higiena). Polski Związek Łowiecki, Warszawa. 16. ŻUCHOWSKA E., 1972 Badania parazytologiczne zwierząt w ogrodach zoologicznych. Medycyna Weterynaryjna 28, 277-280. 17. ŻUCHOWSKA E., 1986 Możliwość badań parazytologicznych w ogrodach zoologicznych. Przegląd Zoologiczny 30, 53-55. 18. ŻUCHOWSKA E., 1987 Znaczenie synantropijnych ptaków krukowatych (Corvidae) w przenoszeniu pasożytów na ptaki hodowane w ZOO. Wiadomości Parazytologiczne 33, 193-198. 19. ŻUCHOWSKA E., 1991 Scabies among the Zoo mammals. Wiadomości Parazytologiczne 37, 123-125. 20. ŻUCHOWSKA E., 1997 Helmintofauna Anseriformes (Aves) z Ogrodu Zoologicznego w Łodzi. Wiadomości Parazytologiczne 43, 213-221. 21. ŻUCHOWSKA E., 1997 Trichurosis bei saugetieren im zoo. Verhandlungsberichte der Enkrankungen der Zootiere 38, 267-269. 149

Justyna Bartosik, Paweł Górski Pasożyty jelitowe wybranych gatunków ssaków przebywających w krajowych ośrodkach hodowli i ekspozycji zwierząt S t r e s z c z e n i e Celem przeprowadzonych badań było określenie składu helmitofauny ssaków przebywających w krajowych ośrodkach hodowli i ekspozycji zwierząt. W okresie od listopada 2006 do czerwca 2007 roku przebadano koproskopowo, metodami flotacji i sedymentacji, 274 próbek kału od 67 gatunków ssaków. Materiał badawczy pochodził od zwierząt z ogrodów zoologicznych w Warszawie, Płocku, Łodzi oraz z Parku Dzikich Zwierząt w Kadzidłowie. Najczęściej odnajdowanymi pasożytami były nicienie z rodziny i Molineidae. Wykryto obecność 9 gatunków pasożytów należących do typu Nematoda oraz trzy pierwotniaki z rodzaju Eimeria. Badania wykazały, że ekstensywność wszystkich inwazji pasożytniczych u badanych zwierząt z ogrodów zoologicznych wynosiła 22-28%, natomiast z Parku Dzikich Zwierząt w Kadzidłowie była znacznie wyższa (48%). Niespotykanym pasożytem u zwierząt udomowionych i jednocześnie potencjalnie groźnym dla ludzi jest glista (Baylisascaris transfuga), której jaja znaleziono w kale niedźwiedzia polarnego. Przeprowadzone badania potraktowano jako wstępne, o charakterze przesiewowym. Uzyskane wyniki pozwoliły na ocenę stanu inwazji pasożytów jelitowych u zwierząt zamieszkujących ogrody zoologiczne centralnej Polski. 150