Abstract
This report represents the prevalence of endoparasitic infections of birds in zoological gardens in Serbia. Coprological examination conducted during 2015 and 2016, involved samples from 318 individual birds belonging to 112 species, in three zoo gardens (Belgrade, Palić and Bor). Individual faeces samples were analysed by the flotation method in salt solution. The presence of endoparasites was established in 51.96% (Belgrade), 46.16% (Palić) and 16.66% (Bor) of the tested birds. We diagnosed coccidian oocysts, eggs of Capillaria spp, Heterakis spp, Trichostrongylus spp, Ascaridia spp, Syngamus trachea and eggs of yet unidentified trematode. There were no detection of parasites from the class of cestodes. Prevalence of infection with coccidia, depending on location, was in the ranges between 8.33% and 32.84%, capillariosis 2.77% and 29.41%, heterakiosis 2.56% and 12.74%, trichostrongylidosis 5.55% and 25.64%, askaridiosis 10.25% and 10.78%, syngamosis 2.94% and trematodes of unknown etiology 2.45%. Coinfections with two or three parasitic species were detected in Belgrade and Palić Zoo Gardens, while quadruple infection was established in birds of Belgrade Zoo Garden. Obtained results can be used in establishing programs for health protection of endangered bird species.
Acknowledgements
This work was funded by the Ministry of Education, Science and Technological Development of the Republic of Serbia.
References
Cano-Terriza D., Guerra R., Lecollinet S., Cerdà-Cuéllar M., Cabezón O., Almería S., García-Bocanegra I. 2015. Epidemiological survey of zoonotic pathogens in feral pigeons (Columba livia var. domestica) and sympatric zoo species in Southern Spain. Comparative immunology, microbiology and infectious diseases, 43, 22–27. 10.1016/j.cimid.2015.10.003Search in Google Scholar PubMed
Collins K.C., Marples M.N. 2015. Zoo Playgrounds: A Source of Enrichment or Stress for a Group of Nearby Cockatoos? A Case Study. Journal of Applied Animal Welfare Science, 18, 375–387. 10.1080/10888705.2015.1034278Search in Google Scholar
Conde D. A., Flesness N., Colchero F., Jones O. R., Scheuerlein A. 2011. An emerging role of zoos to conserve biodiversity. Science, 331, 1390–1391. 10.1126/science.1200674Search in Google Scholar PubMed
Fedynich M.A. 2009. “Heterakis and Ascaridia” in Parasitic Diseases of Wild Birds, C.T. Atkinson, N.J. Thomas and D.B. Hunter, Eds., John Wiley & Sons, Oxford, UK, pp. 388–412. 10.1590/S1984-29612013000200051Search in Google Scholar
Fernandes de Melo M.C., Oliveira B.J., Feitosa F.T., Ribeiro Vilela L.V., Rodrigues Athayde C.A., Medeiros Dantas F.A. et al. 2013. Parasites of Psittaciformes and Accipitriformes in Paraíba state, northeastern Brazil. The Brasilian Journal of Veterinary Parasitology, 22, 314–317. 10.1590/S1984-29612013000200051Search in Google Scholar
Friend M., Franson C.J. 1999. “Intestinal coccidiosis” in Field Manual of Wildlife Diseases-General Field Procedures and Diseases of Birds, M. Friend and J. C. Franson, Eds., U.S. Department of the Interior, U.S. Geological Survey, Biological Resources Division, Information and Technology Report 1999-01, Washington, DC, USA, pp. 207–214Search in Google Scholar
Geraghty V., Mooney J., Pike K. 1982. A study of parasitic infections in mammals and birds at the Dublin Zoological Gardens. Veterinary Research Communication, 5, 343–34810.1007/BF02215003Search in Google Scholar
Godoy S.N. 2007. Psittaciformes (Arara, Papagaio, Periquito). In: Cubas Z.S., Silva J.C.R., Catão-Dias J.L. Tratado de Animais Selvagens. Roca: São Paulo, pp. 222–251Search in Google Scholar
González-Acuña D., Fabry M., Nascimento A.A., Tebaldi J.H. 2007. Death of two slender-billed parakeet (King) (Enicognathus leptorhynchus) (Aves, Psittacidae) by Ascaridia hermaphrodita (Froelich, 1789, Railliet& Henry, 1914) at the National Zoo of Santiago, Chile. Arquoivo Brasilerio Medicina Veterinaria Zootecnia, 59, 539–540. 10.1590/S0102-09352007000200044Search in Google Scholar
Gurler A.T., Beyhan Y.E., Acici M., Bolukbas C.S., Umur S. 2010. Helminths of mammals and birds at the Samsun Zoological Garden, Turkey. Journal of Zoo and Wildlife Medicine, 41, 218–223. 10.1638/2009-0070R1.1Search in Google Scholar
Hofstatter G.P., Guaraldo Aparecida M.A. 2015. Parasitological survey on birds at some selected brazilian zoos. Brazilian Journal of Veterinary Parasitology, 24, 87–91. 10.1590/S1984-29612015005Search in Google Scholar
Illescas Gomez M.P., Rodriguez Osorio M., Arandamaza F. 1993. Parasitation of Falconiform, Strigiform and Passeriform (Corvidae) birds by helminths in Spain. Research and Reviews in Parasitology, 53, 129–135Search in Google Scholar
Kassai T. 1999. Veterinary Helminthology. Butler Worth Heinemann, Oxford, pp. 260. http://dx.doi.org/10.1016/S0169-4758(00)01655-010.1016/S0169-4758(00)01655-0Search in Google Scholar
Lalošević V., Lalošević D., Boboš S., Šinković M., Spasojević Lj. 2007. Intestinal parasites of animals in “Palic” zoo. Contemporary Agriculture, 56, 98–102 (In Serbian). UDK: 616.995.1: 636.025.09(497.113 Palic)Search in Google Scholar
Majewska C.A., Graczyk K.T., Slodkowicz-Kowalska A., Tamang L., Jędrzejewski S., Zduniak P. et al. 2008. The role of free-ranging, captive, and domestic birdsof Western Poland in environmental contaminati on with Cryptosporidium parvumoocysts and Giardia lambliacysts. Parasitology Research, 104, 10931099. 10.1007/s00436-008-1293-9Search in Google Scholar PubMed
Mironov S.V., Palma R.L. 2016. A new feather mite of the genus Trouessartia Canestrini 1899 (Acariformes: Trouessartiidae) from the Seychelles magpie-robin, Copsychus sechellarum (Passeriformes: Muscicapidae). Acta Parasitologica, 61, 629–635. 10.1515/ap-2016-0084Search in Google Scholar PubMed
Morariu S., Todescu L., Dărăbuş G., Morariu F., Ilie M., Stoican M. 2009. Faecal sample screening for endoparasites in zoo parks from Sibiu and Resita – Romania. Revista Romana de Medicina Veterinara 19, 96–114Search in Google Scholar
Murata K. 2002. Prevalence of blood parasites in Japanese wild birds. Journal of Veterinary Medicine Science, 64, 785–79010.1292/jvms.64.785Search in Google Scholar PubMed
Nešić D., Pavlović I., Valter D., Matić G., Hudina V. 1992. Helminths of chamois, mouflon, red deer and roe deer in Belgrade zoo in 1990. Veterinarski Glasnik, 46, 97–101Search in Google Scholar
Nešić D., Pavlović I., Valter D., Savin Z., Hudina V. 1991. Endoparasite fauna of primates at Belgrade zoo. Veterinarski Glasnik, 45, 365–367Search in Google Scholar
Núñez V., Drago F.B., Digiani M.C., Lunaschi L.I. 2017. Nematode parasites of the Chilean Flamingo, Phoenicopterus chilensis (Phoenicopteridae) from Central Argentina, with a description of a new species of Trematoda (Trematidae). Acta Parasitologica, 62, 422–431. 10.1515/ap-2017-0050Search in Google Scholar PubMed
Oliveira J.B., Santos T., Vaughan C., Santiago H. 2011. External parasites of raptors (Falconiformes and Strigiformes): identification in an ex situ population from Mexico. Revista deBiologia Tropical, 59, 1257–1264. 10.15517/rbt.v0i0.3396Search in Google Scholar
Omeragić J., Škapur V., Zuko A. 2003. Parasitofauna of animals and birds in the Sarajevo ZOO. Proceedings of First Symposium of agriculture, veterinary and forestry with international participation, 2003 May 14–17; Neum, BiH; pp. 116–117Search in Google Scholar
Omeragić J., Hodžić A., Zuko Almedina, Jažić A. 2011. Review of investigations of parasitofauna of wild animals in Bosnia and Herzegovina. Veterinaria, 60, 251–257Search in Google Scholar
Otegbade A.C., Morenikeji O.A. 2014. Gastrointestinal parasites of birds in zoological gardens in south-west Nigeria. Tropical Biomedicine, 31, 54–62Search in Google Scholar PubMed
Papini R., Girivetto M., Marangi M., Mancianti F., Giangaspero A. 2012. Endoparasite Infections in Pet and Zoo Birds in Italy, The Scientific World Journal, Volume 2012, Article ID 253127, pp. 9. 10.1100/2012/253127Search in Google Scholar PubMed PubMed Central
Parsani R.H., Momin R.R., Bhuva N.C. 2001. Parasiticinfections among captive birds at Sakkarbagh zoo, Junagadh, Gujarat. Zoos’ Print Journal, 16, 462–464. 10.11609/JoTT.ZPJ.16.4.4624Search in Google Scholar
Patel V.A., Patel I.A., Sahu K.R., Vyas R. 2000. Prevalence of gastrointestinal parasites in captive birds of Gujarat zoos, Zoos’ Print Journal, 15, 295–296. 10.11609/JoTT.ZPJ.14.4.29596Search in Google Scholar
Pavlović I., Hudina V., Kerš V., Blažin V., Šupić V. 1990. Helminth fauna of pheasants in the Belgrade zoo from March to August 1988. Veterinarski Glasnik, 44, 467–471Search in Google Scholar
Pavlović I., Nešić D., Savin Z., Valter D., Hudina V. 1991. Endoparasites of elephant and giraffe in the Belgrade zoological garden. Veterinarski Glasnik, 45, 749–751Search in Google Scholar
Pereira R.J.C. 2007. Falconiformes e Strigiformes (Águia, Gavião, Falcão, Abutre, Coruja). In: Cubas Z.S., Silva J.C.R., Dias J.L.C. Tratado de Animais Selvagens. 2. ed. Roca: São Paulo, pp. 252–267Search in Google Scholar
Pérez Cordón G., Hitos Prados A., Romero D., Sánchez Moreno M., Pontes A., Osuna A., Rosales M.J. 2008. Intestinal parasitism in the animals of the zoological garden “Pena Escrita” (Almuñecar, Spain). Veterinary Parasitology, 156, 302–309. 10.1016/j.vetpar.2008.05.023Search in Google Scholar PubMed
Pérez Cordón G., Hitos Prados A., Romero D., Sánchez Moreno M., Pontes A., Osuna A., Rosales M.J. 2009. Intestinal and haematic parasitism in the birds of the Almunecar (Granada, Spain) ornithological garden. Veterinary Parasitology, 165, 361–36610.1016/j.vetpar.2009.07.027Search in Google Scholar PubMed
Prathipa A., Jayathangaraj G.M., Gomathinayagam S., Thangavelu A. 2013. Endoparasites of Captive Psittacine Birds in Major Zoos in India. Indian Veterinary Journal, 90, 90–91Search in Google Scholar
Radhy M.A., Khalaf M.J., Faraj A.A. 2013. Some gastrointestinal protozoa of zoonotic importance observed in captive animals of Al Zawraa zoo in Baghdad. International Journal of Science and Nature, 4, 567–570Search in Google Scholar
Sanmartín M.L., Álvarez F., Barreiro G., Leiro J. 2004. Helminth fauna of Falconiform and Strigiform birds of prey in Galicia, Northwest Spain. Parasitology Research, 92, 255–263. 10.1007/s00436-003-1042-zSearch in Google Scholar PubMed
Santos T., Oliveira J.B., Vaughann C., Santiago H. 2011. Health of an ex situ population of raptors (Falconiformes and Strigiformes) in Mexico: diagnosis of internal parasites. Revista de Biologia Tropical, 59, 1265–1274. 10.15517/rbt.v0i0.3397Search in Google Scholar PubMed
Sierra C.M., Ramírez F.G., Osorio H.J. 2013. Principale helmintosen contrados en uncentro de fauna cautiva en Columbia. Boetin Cientifico Centro de Museos Museo de Historia Natural, 17, 251–257Search in Google Scholar
Tigin Y., Burgu A., Dogany A., Oge S., Umur S. 1989. Helminthic faecal examination of some mammals and birds in Ankara Zoological Garden. Ankara Universitesi Veteriner Fakultesi Dergisi, 36, 646–664 (In Turkish)Search in Google Scholar
Titilincu A., Mircean V., Bejan A., Iovu A., Ungureanu R., Cozma V. 2009. Prevalence of endoparasites in peacocks (Pavo cristatus). Scientia Parasitologica, 10, 101–105Search in Google Scholar
Tompkins M.D. 2009. “Trichostrongylus,” in Parasitic Diseases of Wild Birds, C.T.Atkinson, N.J.Thomas and D.B.Hunter, Eds., John Wiley & Sons, Oxford, UK, pp. 316–32510.1002/9780813804620.ch17Search in Google Scholar
Tsai S.S., Hirai K., Itakura C. 1992. “Histopathological survey of protozoa”, helminths and acarids of imported and local psittacine and passerine birds in Japan. Japanese Journal of Veterinary Research, 40, 161–174Search in Google Scholar
Víchová B., Reiterová K.,Špilovská S., Blaňarová L., Hurníková Z., Turčeková Ĺ. 2016. Molecular screening for bacteria and protozoa in great cormorants (Phalacrocorax carbo sinensis) nesting in Slovakia, central Europe. Acta Parasitologica, 61, 585–589. 10.1515/ap-2016-0078Search in Google Scholar PubMed
Yabsley J.M. 2009. “Eimeria” in Parasitic Diseases of Wild Birds, Atkinson C.T., Thomas N.J., and Hunter D.B., Eds, John Wiley & Sons, Oxford, UK, pp. 162–18010.1002/9780813804620.ch8Search in Google Scholar
Zhao W.T., Guo Y.N., Zhang L.P., Li L. 2016. Ultrastructure of Ascaridia galli (Schrank, 1788) (Nematoda: Ascaridida) from the endangered green peaflow Pavo muticus Linneatus (Galliformes: Phasianide). Acta Patasitologica, 61, 66–73. 10.1515/ap-2016-0007Search in Google Scholar PubMed
Zuchowska E. 1987. Role of synantropic corvid birds (Corvidae) in the transmission of parasites to zoo birds. Wiadomosci Parazytologiczne, 33, 193–198Search in Google Scholar
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