DOI: 10.2478/s11686-014-0252-0 © W. Stefański Institute of Parasitology, PAS Acta Parasitologica, 2014, 59(3), 363–371; ISSN 1230-2821 The parasitic fauna of the European bison (Bison bonasus) (Linnaeus, 1758) and their impact on the conservation. Part 1 The summarising list of parasites noted Grzegorz Karbowiak*, Aleksander W. Demiaszkiewicz, Anna M. Pyziel, Irena Wita, Bożena Moskwa, Joanna Werszko, Justyna Bień, Katarzyna Goździk, Jacek Lachowicz and Władysław Cabaj W. Stefański Institute of Parasitology, Polish Academy of Sciences, Twarda 51/55, 00-818 Warsaw, Poland Abstract During the current century, 88 species of parasites have been recorded in Bison bonasus. These are 22 species of protozoa (Trypanosoma wrublewskii, T. theileri, Giardia sp., Sarcocystis cruzi, S. hirsuta, S. hominis, S. fusiformis, Neospora caninum, Toxoplasma gondii, Cryptosporidium sp., Eimeria cylindrica, E. subspherica, E. bovis, E. zuernii, E. canadensis, E. ellip- soidalis, E. alabamensis, E. bukidnonensis, E. auburnensis, E. pellita, E. brasiliensis, Babesia divergens), 4 trematodes species (Dicrocoelium dendriticum, Fasciola hepatica, Parafasciolopsis fasciolaemorpha, Paramphistomum cervi), 4 cestodes species (Taenia hydatigena larvae, Moniezia benedeni, M. expansa, Moniezia sp.), 43 nematodes species (Bunostomum trigono- cephalum, B. phlebotomum, Chabertia ovina, Oesophagostomum radiatum, O. venulosum, Dictyocaulus filaria, D.viviparus, Nematodirella alcidis, Nematodirus europaeus, N. helvetianus, N. roscidus, N. filicollis, N. spathiger, Cooperia oncophora, C. pectinata, C. punctata, C. surnabada, Haemonchus contortus, Mazamastrongylus dagestanicus, Ostertagia lyrata, O. ostertagi, O. antipini, O. leptospicularis, O. kolchida, O. circumcincta, O. trifurcata, Spiculopteragia boehmi, S. mathevoss- iani, S. asymmetrica, Trichostrongylus axei, T. askivali, T. capricola, T. vitrinus, Ashworthius sidemi, Onchocerca lienalis, O. gutturosa, Setaria labiatopapillosa, Gongylonema pulchrum, Thelazia gulosa, T. skrjabini, T. rhodesi, Aonchotheca bilobata, Trichuris ovis), 7 mites (Demodex bisonianus, D. bovis, Demodex sp., Chorioptes bovis, Psoroptes equi, P. ovis, Sarcoptes scabiei), 4 Ixodidae ticks (Ixodes ricinus, I. persulcatus, I. hexagonus, Dermacentor reticulatus), 1 Mallophaga species (Bison- icola sedecimdecembrii), 1 Anoplura (Haematopinus eurysternus), and 2 Hippoboscidae flies (Lipoptena cervi, Melophagus ovinus). There are few monoxenous parasites, many typical for cattle and many newly acquired from Cervidae. Keywords Bison bonasus; parasitic protozoa; Trematoda; Cestoda; Nematoda; Acariformes; Ixodidae; Hippoboscidae Introduction was killed. This species’ restitution began in 1929 in the Białowieża Forest. The restitution was possible thanks to spec- The European bison (Bison bonasus) is the largest herbivo- imens purchased from zoological gardens and private animal rous animal in Europe. Historically, the species was distrib- collections. In 1952, the lowland bison was reintroduced to uted throughout western, central and south-eastern Europe, the wildlife area of the Polish section of the Białowieża For- and the Caucasus. Since the Middle Ages, due to hunting and est, as the beginning of the present free-ranging population destruction of the natural forest complexes, the occurrence (Krasińska and Krasiński 2007). Presently, there are over 30 area of European bison dramatically decreased. In the early free-ranging populations located in Poland, Ukraine, Slova- twentieth century, a single free ranging population of Euro- kia, Lithuania, Romania, Belarus and Russia, and many small pean bison was present in the Białowieża Forest. After the groups raised in zoological gardens and show enclosures in First World War, in 1919, the last wild-living European bison Europe. Thus, the present population is composed of closely *Corresponding author: [email protected] 364 Grzegorz Karbowiak et al. related individuals, which affects the health and immunity of 43 species, followed by protozoa – 22 species. Other taxa are these animals. Threats to the health of bison include viral, not numerously represented. The full list of parasite species is bacterial and parasitic diseases (Kita and Anusz 2006; presented in the Table I. Krasińska and Krasiński 2007). The first investigations of infection by internal parasites Parasitic protozoa of European bison were conducted during the early twentieth century. There were recorded in a total of eighteen species of The protozoan parasites are represented by the species belon- parasites, typical for domestic ruminants, apart for two spe- ging to Kinetoplastida (genus Trypanosoma), Diplomonadida cific to bison (Bisonicola sedecimdecembrii and Trypanosoma (genus Giardia) and Apicomplexa (genera Sarcocystis, Neo- wrublewskii) (Wróblewski 1927). In early years, when the Eu- spora, Toxoplasma, Cryptosporidium, Eimeria and Babesia). ropean bisons were present only in captive reserves, only frag- The trypanosomes parasitising in the blood of wild mammals in mentary studies based on small amounts of material the Palaearctic zone are not very well-known. These are the originating from single dissections were conducted. At this species belonging to the Stercorarian group, from the subgen- time, the number of known parasites reached 37 (Dróżdż era Megatrypanum, Herpetosoma and Schizotrypanum. In 1961, 1967). After the restitution of the species, epidemiolog- European bison, two species were recorded: Trypanosoma ical, bacteriological and parasitological studies were con- wrublewskii, Wladimiroff and Yakimoff, 1909, and Try- ducted in the 1950’s, including the study of helminth fauna of panosoma theileri Laveran, 1902. The separation of these animals living in captive breeding reserves, before being re- species is not clear due to their morphological similarity, thus in leased into the wild. These studies followed bison after their 1915, T. wrublewskii was confirmed as a synonym of T. thei- release into open areas, and were repeated after 20 years leri (Yakimoff, 1915). The redescription as the distinct species (Dróżdż et al. 1989, 1994) and are still being conducted. was made at the end of twentieth century (Kingston et al. 1992). In total, the parasitic fauna of European bison is quite well The prevalence of infections in European bison with try- described; however, the knowledge is distracted to the number panosomes is variable, and fluctuates around 15% (Karbowiak of single publications. This work is the first attempt to collect et al. 2006, 2007). Among many parasitic Sarcomastigophora all data to a single publication and to show the phenomena oc- species, only the representatives of Giardia genus are noted curing in the whole parasitic community. in Bison bonasus. The presence of excreted cysts of non-iden- The purpose of this publication is to describe the present tified species has been found in 7.5% of the faecal samples knowledge of the parasite fauna of the European bison B. collected from European bison in the Białowieża Primeval For- bonasus, based on the publications of various scientific centres est (Paziewska et al. 2007). Apicomplexa is the protozoan type that have conducted parasitological studies on these animals, including a large group of small, obligatory parasitic forms. The including those living in free-ranging populations, as well as, apicomplexan parasites of European bison belong to Sarcocys- species bred in zoological gardens and captive breeding re- tidae, Coccidia, Eimeriidae and Piroplasmida. The representa- serves. The overview embraces parasites in the classical mean- tives of Sarcocystidae in the parasite fauna of B. bonasus are ing of this word, so the representatives of protozoan and tissue four species of Sarcocystis genera, Neospora caninum and Tox- animals strictly associated with the bison at least throughout oplasma gondii. Sarcocystis were detected for the first time in one phase of their development, for which the bison is also at the muscle tissue of European bison in the Belarus part of the that time, a habitat of life. It does not include viruses and bac- Białowieża Primeval Forest (Goregliad et al. 1977), later in the teria, being the subject of a microbiological studies, or short- bison kept in the zoological garden in Germany (Odening et al. feeding blood-sucking flies, such as Tabanidae and Culicidae, 1994), and in the heart muscle of the free-living bison in the for which the bison is one of the food sources, and likewise, Polish part of the Białowieża Primeval Forest in 1997 (Osińska the commensally and phoretic mites, nematodes and insects and Piusiński 1997). The percentage of bison infected with Sar- that feed on the bison. We searched the PubMed, ISI Web of cocystis cruzi accounts for 85.4% of the population; however, Science, Scopus and Google Scholar using search terms that this result can be strongly dependent on the diagnostic tech- are associated with the review subject (Bison bonasus, the nique used (Osińska and Piusiński 1997; Pyziel and Demi- names of parasite species, etc.). Moreover, the old papers, that aszkiewicz 2009a). Neospora caninum definitive hosts are are not included in databases, were used. Only the published canine (dog, coyote), however, the parasite has also been de- results obtained during our studies were used, certain unpub- tected in the range of intermediate hosts, livestock and com- lished data are included in the review, if they are required. panion animal species. The antibodies to N. caninum in European bison were reported in 2005,