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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 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 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 (, , Parafasciolopsis fasciolaemorpha, Paramphistomum cervi), 4 cestodes species ( hydatigena larvae, Moniezia benedeni, M. expansa, Moniezia sp.), 43 species (Bunostomum trigono- cephalum, B. phlebotomum, Chabertia ovina, Oesophagostomum radiatum, O. venulosum, 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, axei, T. askivali, T. capricola, T. vitrinus, Ashworthius sidemi, Onchocerca lienalis, O. gutturosa, Setaria labiatopapillosa, pulchrum, gulosa, T. skrjabini, T. rhodesi, Aonchotheca bilobata, ovis), 7 ( bisonianus, D. bovis, Demodex sp., Chorioptes bovis, equi, P. ovis, scabiei), 4 ( ricinus, I. persulcatus, I. hexagonus, reticulatus), 1 Mallophaga species (Bison- icola sedecimdecembrii), 1 Anoplura (Haematopinus eurysternus), and 2 (Lipoptena cervi, ). There are few monoxenous parasites, many typical for and many newly acquired from Cervidae.

Keywords Bison bonasus; parasitic protozoa; ; ; Nematoda; ; 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 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 . 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 ( 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 were present only in captive reserves, only frag- The trypanosomes parasitising in the blood of wild 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 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 (, ), 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, in 7.3% of the animals The review of parasites noted in European bison (Bison examined (Cabaj et al. 2005), but the first direct record was bonasus) noted only in 2010 (Bień et al. 2010). The evidence proved that there was a progressive trend in the prevalence level (Cabaj During the 100 years of investigations conducted by various et al. 2008, 2009, 2010). The presence of T. gondii parasite in centres, there was a total of 88 species of parasites found in European bison has been detected indirectly, using ELISA tests European bison. The most numerous group are nematodes – in 15 of 37 (40.5%) animals (Majewska et al. 2010). The parasites of Bison bonasus – the overwiew 365

Table I. The list of Bison bonasus parasites, with the prevalence noted

Parasite Prevalence Trypanosoma wrublewskii Wladimiroff and Yakimoff, 1909 around 15% (Karbowiak et al. 2006) Trypanosoma theileri Laveran, 1902 **) Giardia spp. 7.5% (Paziewska et al. 2007). Sarcocystis cruzi (Hasselmann, 1923) 85.4% (Osińska and Piusiński 1997; Pyziel and Demiaszkiewicz 2009a) Sarcocystis hirsuta Moulé, 1888 Sarcocystis hominis (Railliet and Lucet, 1891) Sarcocystis fusiformis (Railliet, 1897) **) Neospora caninum Dubey, Carpenter, Speer, Topper and 7–13.4% (Cabaj et al. 2010) Uggla, 1988 Toxoplasma gondii (Nicolle and Manceaux, 1908) 40.5% (Majewska et al. 2010) Cryptosporidium spp. Eimeria cylindrica Wilson, 1931 <2.1%, in calves (Pyziel and Demiaszkiewicz 2009b) Eimeria subspherica Christensen, 1941 <2.1%, in calves (Pyziel and Demiaszkiewicz 2009b) Eimeria bovis Christensen, 1941 23.3% (Pyziel and Demiaszkiewicz 2009b) Eimeria zuernii Rivolta, 1878 4.2% (Pyziel and Demiaszkiewicz 2009b) Eimeria canadensis Bruce, 1921 <2.1% (Pyziel and Demiaszkiewicz 2009b) Eimeria ellipsoidalis Becker and Frye, 1929 <2.1% (Pyziel and Demiaszkiewicz 2009b) Eimeria alabamensis Christensen and Porter, 1939 <2.1% (Pyziel and Demiaszkiewicz 2009b) Eimeria bukidnonensis Tubangui, 1931 <2.1% (Pyziel and Demiaszkiewicz 2009b) Eimeria auburnensis Christensen and Porter, 1939 <2.1% (Pyziel and Demiaszkiewicz 2009b) Eimeria pellita Supperer, 1952 <2.1% (Pyziel and Demiaszkiewicz 2009b) Eimeria brasiliensis Torres and Ramos, 1939 <2.1% (Pyziel and Demiaszkiewicz 2009b) Babesia divergens (M’Fadyean and Stockman, 1911) 33% (Karbowiak et al. 2004) Fasciola hepatica Linnaeus, 1758 44–50% (Dróżdż et al. 1989) to 100% (Demiaszkiewicz and Pyziel 2010) Parafasciolopsis fasciolaemorpha Ejsmont, 1932 20–27% (Demiaszkiewicz and Pyziel 2010) Paramphistomum cervi (Zeder, 1790) 23–25% (Dróżdż et al. 1989; Demiaszkiewicz 2005) Dicrocoelium dendriticum (Rudolphi, 1819) 16 to 41% (Dróżdż et al., 1989; Demiaszkiewicz and Pyziel 2010) Moniezia benedeni (Moniez, 1879) 41% (Demiaszkiewicz 2005) (Rudolphi, 1805) **) Moniezia sp. single specimen (Dróżdż 1961) Pallas, 1766 *) Bunostomum trigonocephalum (Rudolphi, 1808) Bunostomum phlebotomum (Railliet, 1900) **) Chabertia ovina (Gmelin, 1790) 2–5 % (Dróżdż et al. 1989; Demiaszkiewicz et al. 2010; Demiaszkiewicz and Pyziel 2010) Oesophagostomum radiatum (Rudolphi, 1803) 2–5 % (Dróżdż et al. 1989; Demiaszkiewicz et al. 2010; Demiaszkiewicz and Pyziel 2010) Oesophagostomum venulosum (Rudolphi, 1809) 100% (Demiaszkiewicz et al. 2012) Dictyocaulus filaria (Rudolphi, 1809)**) Dictyocaulus viviparus (Bloch, 1782) 94% of calves, 26% of older (Demiaszkiewicz and Pyziel 2010) Nematodirella alcidis Dikmans, 1935 < 3% (Dróżdż et al. 1989) Nematodirus europaeus Jansen, 1972 Nematodirus helvetianus May, 1920 < 10% (Dróżdż et al. 1989; Demiaszkiewicz et al. 2010; Demiaszkiewicz and Pyziel 2010) Nematodirus roscidus Railliet, 1911 40–60% (Dróżdż et al. 1989; Demiaszkiewicz et al. 2010) Nematodirus filicollis (Rudolphi, 1802) **) Nematodirus spathiger (Railliet, 1896) **) Cooperia oncophora (Railliet, 1898) 90–100% (Dróżdż et al. 1989, 1994, 2002; Demiaszkiewicz and Pyziel 2010; Demiaszkiewicz et al. 2012) Cooperia pectinata Ransom, 1907 Cooperia punctata (Linstow, 1906) 20–50% (Dróżdż et al. 1989, 1994, 2002; Demiaszkiewicz and Pyziel 2010; Demiaszkiewicz et al. 2012) Cooperia surnabada Antipin, 1931 366 Grzegorz Karbowiak et al.

Haemonchus contortus (Rudolphi, 1802) Mazamastrongylus dagestanicus (Altaev, 1953) Ostertagia lyrata Sjoberg, 1926 Ostertagia ostertagi (Stiles, 1892) 90–100% (Dróżdż et al. 1989, 1994, 2002; Demiaszkiewicz and Pyziel 2010; Demiaszkiewicz et al. 2012) Ostertagia antipini Matschulski, 1950 Ostertagia leptospicularis Assadov, 1953 90–100% (Dróżdż et al. 1989, 1994, 2002; Demiaszkiewicz and Pyziel 2010; Demiaszkiewicz et al. 2012) Ostertagia kolchida Popova, 1937 90–100% (Dróżdż et al. 1989, 1994, 2002; Demiaszkiewicz and Pyziel 2010; Demiaszkiewicz et al. 2012) Ostertagia circumcincta (Stadelmann, 1894) Ostertagia trifurcata Ransom, 1907 Spiculopteragia boehmi Gebauer, 1932 90–100% (Dróżdż et al. 1989, 1994, 2002; Demiaszkiewicz and Pyziel 2010; Demiaszkiewicz et al. 2012) Spiculopteragia mathevossiani Ruchljadev, 1948 20–50% (Dróżdż et al. 1989, 1994, 2002; Demiaszkiewicz and Pyziel 2010; Demiaszkiewicz et al. 2012) Spiculopteragia asymmetrica (Ware, 1925) Trichostrongylus axei (Cobbold, 1879) 20–50% (Dróżdż et al. 1989, 1994, 2002; Demiaszkiewicz and Pyziel 2010; Demiaszkiewicz et al. 2012) Trichostrongylus askivali Dunn, 1964 Trichostrongylus capricola Ransom, 1907 Trichostrongylus vitrinus Looss, 1905 Ashworthius sidemi Schulz, 1933 100%, in the last decade (Demiaszkiewicz and Pyziel 2010) Onchocerca gutturosa Neumann, 1910 35% (Dróżdż et al. 1989; Demiaszkiewicz et al. 2007) Onchocerca lienalis (Stiles, 1892) 71% (Dróżdż et al. 1989; Demiaszkiewicz et al. 2007) Setaria labiatopapillosa (Alessandrini, 1838) 25 to 71% (Dróżdż et al. 1989; Demiaszkiewicz and Pyziel 2010) Molin, 1857 Thelazia gulosa (Railliet and Henry, 1910) 28% (Gagarin and Nazarova 1966; Dróżdż et al. 1989; Demiaszkiewicz and Pyziel 2010) Thelazia skrjabini Erschov, 1928 28% (Gagarin and Nazarova 1966; Dróżdż et al. 1989; Demiaszkiewicz and Pyziel 2010) Thelazia rhodesi (Desmarest, 1822) **) Aonchotheca bilobata (Bhalerao, 1933) 22–70% (Dróżdż et al. 1989; Demiaszkiewicz and Pyziel 2010) Trichuris ovis (Abildgaard, 1795) 43 to 100% (Gagarin and Nazarova 1966; Dróżdż et al. 1989, Demiaszkiewicz et al. 2010) Demodex bisonianus Kadulski and Izdebska, 1996 (Stiles, 1892) 50% (Kadulski and Izdebska 1996; Izdebska 2001b, 2006) Demodex sp. **) – Chorioptes bovis (Hering, 1845) 50% (Izdebska 2001 a,b) Psoroptes equi (Hering, 1838) **) Psoroptes ovis (Hering, 1898) single record (Kadulski et al. 1996; Izdebska 2001a, b) Latreille, 1802 **) Ixodes ricinus Linnaeus, 1758 common (Kadulski et al. 1996) Ixodes persulcatus Schultze, 1930 **) Ixodes hexagonus Leach, 1815 **) Fabricius, 1794 reaches 100% (Izdebska 2001 b, Karbowiak et al. 2003) Bisonicola sedecimdecembrii (Eichler, 1946) 37 to 54% (Izdebska 2001 a,b, 2003) Haematopinus eurysternus (Nitzsch, 1818) **) Lipoptena cervi Linnaeus, 1758 single records (Kadulski et al. 1996) Melophagus ovinus **)

*)in B. bonasus larval forms only. **)the permanent occurrence in B. bonasus not confirmed presently.

Cryptosporidium spp. has a broad spectrum of hosts, and many, the cysts were detected in bison kept in zoological gar- was recorded in many species of ruminants, rodents and car- dens (Jakob 1992). The coccidian of Eimeria genus are para- nivores, as well as domestic animals. The presence of oocysts sitic protozoa, common among domestic and wild and and DNA of non-identified species of Cryptosporidium were mammals. There are 11 Eimeria species, recorded in Euro- found in 29 faecal samples of European bison collected in the pean bison, all previously recorded from cattle. The predom- Białowieża Primeval Forest (Paziewska et al. 2007). In Ger- inant species of European bison is E. bovis (prevalence The parasites of Bison bonasus – the overwiew 367

23.3%), followed by E. zuernii (4.2%), the other species occur bison living free in the Białowieża Forest – M. expansa and M. rarely, their prevalence does not exceed 2.1% (Pyziel et al. benedeni. The first species is relatively rare and in some years 2011). Moreover, apart Eimeria finding in bisons free-living in absent. M. benedeni seems to be the proper parasite of this Białowieża Primeval Forest, E. bovis has also been noted in ruminant, apart from the Białowieża Forest, their presence is Bulgaria (Golemansky 2003). Non-identified Eimeria was confirmed in other localities (Gagarin and Nazarova 1966) and found in free-ranging bison living in the Vânâtori-Neamt Nat- also in zoological gardens (Jaros et al. 1966). This cestoda was ural Park in Romania (Petrovici and Petrovici 2005). recorded in 41% of the animals studied, and more often among Among some species of Babesia occurring in Europe, only them in calves. Moreover, the non-identified tapeworm from Babesia divergens was recorded in European bison. The this genus, but morphologically different, has been found in prevalence of infection was found in 33% of bison studied animals living in the Borecka Forest (northern Poland) (Karbowiak et al. 2004). (Dróżdż 1961; Demiaszkiewicz et al. 2008). The definitive hosts of Taenia hydatigena species are Carnivores. The larval Trematodes forms were detected in tissues of wild living bison; however, they are not found in enclosure animals (Dróżdż et al. 1989; Trematodes are common parasites of domestic and wild Demiaszkiewicz 2005). mammals, as well as birds. However, only four species were found in B. bonasus. F. hepatica and D. dendriticum are Nematodes known in European bison as the mainspring of these animals mortality at the turn of the nineteenth/twentieth century. At Nematodes is the biggest and the best studied group of inter- the beginning of the twentieth century, Wróblewski (1927) nal parasites of European bison. Presently (in 2013), there are showed F. hepatica as one of the dominants parasites of 43 species of parasitic nematodes recorded from farmed and bison. During the reintroduction of bison after the Second free-living bisons. These are the representatives of the orders World War, the fluke was rarely recorded (Dróżdż 1961, (genera Bunostomum, Chabertia, Oesophagosto- 1967). However, from the 1950s until the end of the twenti- mum, Dictyocaulus, Nematodirella, Nematodirus, Cooperia, eth century, their prevalence slowly increased to 44%–50% of Haemonchus, Mazamastrongylus, Spiculopteragia, Osterta- bison (Dróżdż et al. 1989) and in the recent decade reached gia, Trichostrongylus, Ashworthius) (genera On- almost 100% (Demiaszkiewicz and Pyziel 2010). D. den- chocerca, Setaria, Gongylonema, Thelasia) and Enoplida driticum was also recorded in the Białowieża Forest by (genera Aonchoteca, Trichuris). Ancylostomatidae con- Wróblewski (1927); however their prevalence was never so tains two representatives. Bunostomum trigonocephalum is a high, it was variable, from 16% to 41% of the hosts (Dróżdż typical parasite for elk (Alces alces), which however, are noted et al. 1989; Demiaszkiewicz and Pyziel 2010). F. hepatica, in bison in the Bialowieża Forest as recently as the 1950s, as D. dendriticum and the next fluke – Paramphistomum cervi well as in populations studied in Russia (Dróżdż 1961; – were also detected in bisons living in Russian reserves Gagarin and Nazarova 1966). B. phlebotomum is a parasite (Gagarin and Nazarova 1966). P. cervi is the parasite typical typical for cattle, in B. bonasus, it was recorded in semi-free for cattle. The prevalence of infection in B. bonasus ranges populations in Russia (Gagarin and Nazarova 1966). from 23% to 25% (Dróżdż et al. 1989; Demiaszkiewicz There are three representative species of the Chabertiidae fam- 2005). The last fluke, P. fasciolaemorpha is the parasite typ- ily in B. bonasus, all typical cattle parasite (Demiaszkiewicz ical for elk (Alces alces) and common also in other cervidae. and Pyziel 2010). The most common is Oesophagostomum It was recorded for the first time in European bison in the venulosum, parasitising almost 100% of the animals studied years 1983–86, in about 6% of the animals investigated (Demiaszkiewicz et al. 2012). The prevalence of infection (Dróżdż et al. 1989). Since then, the prevalence of infection with the other species is somewhere around 2%–5% of bisons has slowly increased, to 20%–27%; however, the intensity (Dróżdż et al. 1989; Demiaszkiewicz et al. 2010; Demi- and pathogenicity remains relatively low (Demiaszkiewicz aszkiewicz and Pyziel 2010). Chabertia ovina, with the and Pyziel 2010). exception of free-living population in the Białowieża Forest (Dróżdz et al. 1990) was noted in bison kept in zoological Cestodes gardens and semi-free populations (Gagarin and Nazarova 1966; Jaros et al. 1966). The Dictyocaulidae family, consist- Cestodes are common parasites of every group, and ing of two representatives of Dictyocaulus genus – D. vivipa- also in its larval form in many . Thus, they play rus and D. filaria – are noted in B. bonasus. D. viviparus is an important role also as parasites of bison. There are four more often recorded (Demiaszkiewicz and Pyziel 2010). This species of cestodes noted in B. bonasus, belonging to the species was also found in free-ranging bison living in the and Taenidae families (Demiaszkiewicz Vânâtori-Neamt Natural Park in Romania and many reserves 2005), represented by genera Moniezia and Taenia. in Russia (Gagarin and Nazarova 1966; Petrovici and Petro- Moniezia tapeworms are common parasites of ruminants. vici 2005). The previous records and occurrence of D. filar- The detailed studies showed the presence of two species in ia currently require confirmation. The Molineidae family con- 368 Grzegorz Karbowiak et al.

tains six species present in B. bonasus. Nematodirella alcidis, tioned as a parasite of B. bonasus by Gagarin and Nazarova Nematodirus europaeus and N. roscidus are parasites typical (1966) and Anderson (2000); however, their presence in ani- for Cervidae, and in bison relatively rare; the prevalence of mals living in the natural environment is not confirmed. infection does not exceed 3% (Dróżdż et al. 1989). N. helve- family includes two species found in European tianus is typical for the cattle parasite (Dróżdż et al. 1989; bison. Aonchotheca bilobata originates from southeastern Demiaszkiewicz et al. 2010; Demiaszkiewicz and Pyziel Asia, and were transferred to European bison probably in zo- 2010). The high prevalence and intensity of infection (40% – ological gardens (Dróżdż et al. 1989; Demiaszkiewicz and 60% of bisons investigated) were observed for N. roscidus. Pyziel 2010). Trichuris ovis is native species, recorded in 43% N. helvetianus was recorded in bison in Russia (Gagarin and to 100% of free-living animals (Gagarin and Nazarova 1966; Nazarova 1966), N. filicollis and N. spathiger were noted Dróżdż et al. 1989, Demiaszkiewicz et al. 2010). once, in close animal husbandry in Sweden (Koffman 1942). The Trichostrongylidae is the very important family of nema- Mites todes parasite in B. bonasus; it includes 20 species recorded in this host. The most common species are Cooperia oncophora, The subclass includes the number of very diverse arthro- Ostertagia leptospicularis, O. kolchida, O. ostertagii and pods, among them, many parasites of various groups. Spiculopteragia boehmi, followed by C. punctata, S. math- In European bison, the infections were recorded within repre- evossiani, Trichostrongylus axei (Dróżdż et al. 1989, 1994, sentatives of the families (genus Demodex), 2002; Demiaszkiewicz and Pyziel 2010; Demiaszkiewicz et (genera Chorioptes and Psoroptes) al. 2012). The majority of Trichostrongylidae are typical for (genus Sarcoptes) and Ixodidae (genera Ixodes and Derma- Cervidae or are parasites found in many groups of ruminants. centor). Demodex bovis is a typical parasite of cattle, there- O. ostertagi and O. circumcincta were noted also in farm bison fore their occurrence in European bison is rare, and their in Sweden (Koffman 1942), and with C. oncophora, C. punc- findings are limited to Białowieża (Izdebska 2001b). D. biso- tata, Haemonchus contortus in semi-free living in Russia nianus is one of the specific parasites for B. bonasus, and most (Gagarin and Nazarova 1966), H. contortus and T. axei in frequent and abundant (Kadulski and Izdebska 1996; Izdebska Prague (Jaros et al. 1966). H. contortus, O. circumcincta, T. vit- 2001b, 2006). The third species, Demodex sp., is different, but rinus also in free-ranging bison living in the Vânâtori-Neamt due to its low prevalence and a small number of individuals it Park in Romania (Petrovici and Petrovici 2005). The remark- is not identified by authors (Izdebska 2006). Psoroptidae in- able species is Ashworthius sidemi. It was found for the first cludes the cosmopolitan , which occurred on domestic ru- time in Poland in February 1997 in bisons from the Bi- minants, as well as wild mammals. Chorioptes bovis is one of ałowieża-Caucasus line living in the wild in the Bieszczady the most frequent and abundant mites in European bison Mountains. Later it appeared in other bison populations (Izdebska 2001 a,b). Psoroptes equi is the parasite of the (Demiaszkiewicz et al. 2009). The sources of the parasites , but is found in free-ranging populations and those ani- were red deer, which brought the parasite from neighbouring mals dwelling in the reserve. P. ovis is the parasite of Ukraine and Slovakia (Dróżdż et al. 1998, 2002). and , with worldwide spreading. It has been found only From the Onchocercidae family, there are three species once, in the reserve bison in Białowieża (Kadulski et al.1996; recorded in European bison. Onchocerca gutturosa is found Izdebska 2001a,b) Sarcoptidae is the family of mites adapted in 35% of the animals studied, and O. lienalis and Setaria labi- to living in the skin of mammals. Sarcoptes scabiei is a spe- atopapillosa are recorded more often, the prevalence of in- cific parasite of , however, it can be transmitted to fection reaches 71% of the bisons studied (Dróżdż et al. 1989; many species of domestic animals and subsequently to wild Demiaszkiewicz et al. 2007). Moreover, the prevalence of in- hosts. This parasite was recorded only once in the reserve fections with S. labiatopapillosa slowly increased, from 25% bison only and their occurrence in free-living animals is dis- (1983–86) to 71% of the animals studied (2006–2007) putable (Izdebska 2001 a,b). From the Ixodidae family, the (Dróżdż et al. 1989; Demiaszkiewicz and Pyziel 2010). presence of four species was noted. Ixodes ricinus is a Gongylonematidae family is represented by one species common parasite of European bison kept in captive breeding recorded in B. bonasus – Gongylonema pulchrum. That para- reserves and often noted in the bison from free-ranging herds site was found in wild-living bison in the Białowieża Forest (Kadulski et al. 1996). Ixodes persulcatus and I. hexagonus (Wróblewski 1927), later in semi-free bison in Khoperskii Za- were recorded only once, in the Białowieża Forest in speci- povednik in Russia, and was not detected in enclosure animals mens in a captive reserve (Kadulski et al. 1996; Izdebska (Gagarin and Nazarova 1966; Demiaszkiewicz and Pyziel 2001b). Infections with these two tick species are most likely 2010). Similarly, from the Thaelaziidae family, only one genus incidental, because I. persulcatus is a very rare species in was recorded for B. bonasus – Thelazia, with three species Poland, and I. hexagonus is the parasite typical in for hedge- parasitising B. bonasus. T. gulosa and T. skrjabini were found hog. Apart of the single report, their presence in the bison was in 28% of free-living animals in Polish and Belarus parts of the not confirmed. The Dermacentor reticulatus tick is a common Białowieża Forest (Gagarin and Nazarova 1966; Dróżdż et al. parasite of European bison (Izdebska 2001 b), and in the big 1989; Demiaszkiewicz and Pyziel 2010). T. rhodesi is men- numbers overwinters on this host (Karbowiak et al. 2003). The parasites of Bison bonasus – the overwiew 369

Insects Acknowledgements. Data unpublished earlier were obtained in MNISW grant no N308 234738 and NCN grant no. N N308 563840. Insecta is the large class of invertebrates, including many par- asitic species. In light of their number and diversity, the num- ber of parasite species connected with Bison bonasus is References surprisingly low. They belong to orders Mallophaga (genus Bisonicola), Anoplura (genus Haematopinus), and Diptera Anderson R.C. (Ed.). 2000. parasites of . Their development and transmission, second ed. CABI Publishing, (genera Lipoptena, Melophagus). Wallingford, UK, 650 p From Mallophaga, one species is noted in European bison Bień J., Moskwa B., Cabaj W. 2010. In vitro isolation and identifi- – Bisonicola sedecimdecembrii. It is the specific parasite of cation of the first Neospora caninum isolate from European the genus Bison. Currently, it seems to be the common para- bison (Bison bonasus bonasus L.). Veterinary Parasitology, sites of the European bisons population (Izdebska 2001 a,b, 173, 200–205. DOI: 10.1016/j.vetpar.2010.06.038. Burlinski P., Janiszewski P., Kroll A., Gonkowski S. 2011. Parasito- 2003, 2011). fauna in the gastrointestinal tract of the cervids (Cervidae) in The Anoplura consists of the obligatory external northern Poland .Acta Veterinaria (Beograd), 61, 269–282. blood-feeding parasites of mammals. In B. bonasus, one DOI: 10.2298/AVB1103269B species is known – Haematopinus eurysternus. It was recorded Cabaj W., Bień J., Goździk K., Moskwa B. 2009. Neospora caninum in the European bison at the beginning of the twentieth cen- u żubrów w Polsce – aktualny stan badań. European bison conservation: newsletter, 2, 102–111. tury by Wróblewski (1927), but at present it is not found. Cabaj W., Bień J., Goździk K., Moskwa B. 2010. Neospora caninum Dipteran, coming from the family Hippoboscidae, is the u żubrów żyjących w Białowieży. European bison conserva- obligate parasites of mammals and birds. In the European tion: newsletter, 3, 63–68. bison, there were two species found. Lipoptena cervi is the Cabaj W., Goździk K., Bień J., Moskwa B. 2008. Neospora caninum common parasite of Cervidae and wild boars, and other hosts u żubrów – świadomość problemu. European bison conser- vation: newsletter, 1, 53–64. attack incidentally. It was noted in B. bonasus in captive re- Cabaj W., Moskwa B., Pastusiak K., Gill J. 2005. Antibodies to serve in Niepołomice (Izdebska 2001b), and a single speci- Neospora caninum in the blood of European bison (Bison men was also found on free-living animals in the Białowieża bonasus bonasus L.) living in Poland. Veterinary Parasitology, Forest (Kadulski et al. 1996). Melophagus ovinus is a specific 128, 163–168. DOI: 10.1016/j.vetpar.2004.09.033 sheep and parasite, and its occurrence in other hosts is Demiaszkiewicz A.W. 2005. Helminty i wywoływane przez nie helminthozy dzikich przeżuwaczy. Kosmos, 54, 61–71. coincidental. It was noted by Wróblewski (1927), and it was Demiaszkiewicz A.W., Lachowicz J., Karbowiak G. 2007. Increase currently found in the reserve bison only (Izdebska 2001 a,b). of infection level of European bison by nematodes Setaria labiatopapillosa in Białowieża Forest. Wiadomości Parazy- Conclusion tologiczne, 53 (suppl.), 17. Demiaszkiewicz A.W., Lachowicz J., Osińska B. 2009. Nowe ogni- sko aswortiozy dzikich przeżuwaczy w Puszczy Białowie- In total, the number of parasites recorded in European bison – skiej. Magazyn Weterynaryjny, 18, 355–357. 88 species – is big in comparison to parasites noted in closely Demiaszkiewicz A.W., Pyziel A.M. 2010. Forming of European related American bison (Bison bison) (Tessaro 1989) and other bison helminth fauna in Białowieża Forest. In: (Eds. R. ruminants cohabitating the same area – elk (Alces alces), fal- Kowalczyk, D Ławreszuk and J.M. Wójcik.) Ochrona żubra low deer (Dama dama) and red deer (Cervus elaphus) (Dróżdż w Puszczy Białowieskiej. Zagrożenia i perspektywy rozwoju populacji. ZBS PAN,:Białowieża, 63–74. et al. 1997; Demiaszkiewicz 2005; Burlinski et al. 2011; Demiaszkiewicz A.W., Pyziel A.M., Kuligowska I., Lachowicz J. Kowal et al. 2012). 2010. Parazytozy żubrów powodowane przez nicienie lokali- There are evident few number of monoxenous parasites zujące się w jelicie grubym. European bison conservation: specific for European bison. These are Trypanosoma newsletter, 3, 69–75. wrublewskii, Bisonicola sedecimdecembrii and Demodex Demiaszkiewicz A.W., Pyziel A.M., Kuligowska I., Lachowicz J., Krzysiak M. K. 2012. Nematodes of the large intestine of the bisonianus. There are many parasites typical to cattle, and European bison of the Białowieża National Park. Annales of many new parasite species acquired from Cervidae. This fact Parasitology, 58, 9–13. can be connected with the dramatic history of the B. bonasus Demiaszkiewicz A.W., Pyziel A.M., Lachowicz J. 2008. Stan zara- species, restituted from some specimens bred in captive żenia żubrów helmintami w Puszczy Białowieskiej w sezo- farms. Other characteristic facts are the increased trend in bio- nie zimowym 2007/2008. European bison conservation: newsletter, 1, 42–52. diversity of parasites, as well as in prevalence and inten- Dróżdż J. 1961. A study on helminths and helminthiases in bison, Bison sity of infections. The number of reports of significant foreign bonasus (L.) in Poland. Acta Parasitologica Polonica 9, 55–95. and indigenous pathogens in European bison illustrate the im- Dróżdż J. 1967. The state of research on the helminthofauna of the portance of controlling diseases and the safeguarding of the European bison. Acta Theriologica, 12, 377–384. bison populations. Fatalities can be attributed to many para- Dróżdż J., Demiaszkiewicz A.W., Lachowicz J. 1989. The helminth fauna of free-ranging European bison Bison bonasus L. Acta sitoses, especially caused by newly acquired parasites as Ash- Parasitologica Polonica, 34, 117–124. wortius sidemi and Neospora caninum (Dróżdż et al. 1998; Dróżdż J., Demiaszkiewicz A.W., Lachowicz J. 1994. The helminth Cabaj et al. 2008). fauna of free-ranging European bison, Bison bonasus (L), 370 Grzegorz Karbowiak et al.

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Received: October 2, 2013 Revised: January 13, 2014 Accepted for publication: March 28, 2014