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Home , European bison, Melophagus, Moniezia, Psoroptidae, Thelazia

DOI: 10.2478/s11686-014-0253-z © W. Stefański Institute of Parasitology, PAS Acta Parasitologica, 2014, 59(3), 372–379; ISSN 1230-2821 The parasitic fauna of the European (Bison bonasus) (Linnaeus, 1758) and their impact on the conservation. Part 2 The structure and changes over time

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,

Abstract During the last century the recorded parasite fauna of Bison bonasus includes 88 . These are 22 species of protozoa, 4 trematode species, 4 cestode species, 43 species, 7 , 4 , 1 Mallophaga species, 1 Anoplura, and 2 . There are few monoxenous parasites, the majority of parasites are typical for other and Cervidae species and many are newly acquired from Cervidae. This is an evident increased trend in the parasite species richness, in both the prevalence and intensity of infections, which is associated with the bison population size, host status ( or free-ranging) and the possibility of contact with other species. In light of the changes to parasite species richness during the last decades, special emphasis shall be given to new parasite species reported in , their pathogenicity and potential implications for conservation.

Keywords Bison bonasus, parasite

Introduction their release into the wild, was repeated after 20 years (Dróżdż et al. 1989, 1994), and is still being conducted. The European bison (Bison bonasus) is the largest herbivo- Summarising the publications available, the parasite fauna rous in . Due to their dramatic history, their of European bison is quite well described; however, most re- present population is composed of closely related individuals, ports of parasites in B. bonasus are based on small numbers of a fact that affects the health and immunity of these bison from isolated single populations or zoological gardens. (Kita and Anusz 2006; Krasińska and Krasiński 2007). Threats Therefore, the prevalence, geographical distribution and to the health of bison include viral, bacterial and parasitic dis- clinical significance of most parasites cannot be widely inter- eases. The first investigations into parasites of European bison preted. The full list of all B. bonasus parasites is presented in were conducted during the early twentieth century. In early the first part of the review; part 2 describes phenomena years, when the European bison were present only in the occurring in the whole parasitic fauna of B. bonasus – changes captive reserves, only fragmentary studies based on small of the parasite fauna after the to the wild amounts of material originating from single dissections were and aquisition of new parasite species. conducted; however, the number of known parasite species The purpose of this publication is to describe the present reached at this time 37 (Dróżdż 1961, 1967). After the resti- knowledge of the parasite fauna of the European bison tution of the species, an epidemiological, bacteriological and B. bonasus, based on the publications of various scientific parasitological study began in the 1950’s, including study of centres that have conducted parasitological studies on this helminth fauna of animals living in captive breeding reserves animal, includes on those living in free-ranging populations before they were released. This study followed bison after as well as bred in zoological gardens and captived reserves.

*Corresponding author: [email protected] The parasitic fauna of Bison bonasus 373

The analysis of the parasite fauna and their changes during , recorded in 43 to 100% of bison. Also recent decades was conducted on the basis of the available Ixodidae ticks are common parasites, found in almost every literature data as well as our own observations. free-living bison. Other parasites are subdominant, found in up to 20% of studied, with prevalence levels up to The diversity and structure of B. bonasus parasite fauna 1–3% of population. In view of the hosts preferences, the most common para- On the basis of publications describing parasitological studies site group observed in bison are the parasites shared with - made in the natural environment, as well as those describing tle – these include the apicomplexan parasites from the genera cases of infections in captive-breeding European bison, it is Sarcocystis and Eimeria, a single species of fluke, tapeworm possible to establish a list of parasites associated with the an- and , and 14 species of . The group of parasites imal, and the changes in the parasite fauna from the beginning that infect a range of Bovidae species, among them species of the twentieth century, across the critical beginning of resti- having the preference for , include 9 species of tution, to the current state of a stable free-living population of helminths, the protozoan parasite Babesia bovis and the mite bison at the beginning of the twenty-first century. The full list . All these species can be typical parasites of of taxa and parasite species is presented in the first part of the B. bonasus due to the close relationship of bison to and publication (Karbowiak et al. 2014). other Bovidae. In summary, during the past 100 years there have been The next group are parasites specific for Cervidae. These 88 species of parasites found, more or less associated with include 17 species, including one fluke and 16 species of ne- European bison. The most numerous group are the nematodes matodes. Some of these species may possibly be parasites pri- – 43 species, followed by protozoa – 22 species (Fig. 1). marily shared with cervidae, however, most of them are new Almost all parasites are polyxenic, have a large range of species received from . Parafasciolopsis fasciolaemor- hosts, or are shared with other wild ungulates or cattle (Kita pha, capricola, Ostertagia leptospicularis, and Anusz 2006; Krasińska and Krasiński 2007). Only 3 Ostertagia kolchida, Spiculopteragia mathevossiani, Coope- species parasitising B. bonasus are monoxenous parasites of ria pectinata, Nematodirus europaeus and Nematodirus this host: Trypanosoma wrublewskii, Bisonicola sedecimde- roscidus were aquired by bison from deer during the second cembrii and Demodex bisonianus (Table I). part of twentieth century (Dróżdż et al. 1989), while the nem- Currently the most common parasites of B. bonasus are atode Spiculopteragia asymmetrica was recorded in bison for nematodes belong to the Trichostrongylidae – these are the first time in 1992 (Dróżdż et al. 1994). This phenomena C. oncophora, O. leptospicularis, Ostertagia kolchida, O. os- can be related to the increase of red and roe deer numbers in tertagii, and S. boehmi, for which the prevalence level reaches Białowieża forest and contact of the restituted population of 90–100%. They are followed by Trichuris ovis and the fluke European bison with deer. Especially noticeable are the para-

Fig 1. The structure of parasite fauna of European bison Bison bonasus; the taxonomic groups 374 Grzegorz Karbowiak et al.

Table I. The definitive hosts of the Bison bonasus parasites. The parasites needed confirmation and/or single recorded not mentioned

Main host Parasite Bison bonasus specific parasites Trypanosoma wrublewskii Wladimiroff and Yakimoff, 1909 Demodex bisonianus Kadulski and Izdebska, 1996 Bisonicola sedecimdecembrii (Eichler, 1946)

Bos taurus Sarcocystis cruzi (Hasselmann, 1923) S. hirsuta Moulé, 1888 S. hominis (Railliet and Lucet, 1891) Eimeria cylindrica Wilson, 1931 E. subspherica Christensen, 1941 E. bovis Christensen, 1941 E. zuernii Rivolta, 1878 E. canadensis Bruce, 1921 E. ellipsoidalis Becker and Frye, 1929 E. alabamensis Christensen and Porter, 1939 E. bukidnonensis Tubangui, 1931 E. auburnensis Christensen and Porter, 1939 E. pellita Supperer, 1952 E. brasiliensis Torres and Ramos, 1939 Paramphistomum cervi (Zeder, 1790) Moniezia benedeni (Moniez, 1879) Chabertia ovina (Gmelin, 1790) Oesophagostomum radiatum (Rudolphi, 1803) Oe. venulosum (Rudolphi, 1809) Nematodirus helvetianus May, 1920 Cooperia oncophora (Railliet, 1898) C. punctata (Linstow, 1906) C. surnabada Antipin, 1931 Haemonchus contortus (Rudolphi, 1802) Ostertagia lyrata Sjoberg, 1926 Onchocerca gutturosa Neumann, 1910 O. lienalis (Stiles, 1892) Setaria labiatopapillosa (Alessandrini, 1838) Thelazia gulosa (Railliet and Henry, 1910) Th. skrjabini Erschov, 1928 Demodex bovis (Stiles, 1892)

Alces alces Parafasciolopsis fasciolaemorpha Ejsmont, 1932 Bunostomum trigonocephalum (Rudolphi, 1808) Nematodirella alcidis Dikmans, 1935 Mazamastrongylus dagestanicus (Altaev, 1953) Trichostrongylus capricola Ransom, 1907

Cervidae, number of host species Nematodirus europaeus Jansen, 1972 N. roscidus Railliet, 1911 C. pectinata Ransom, 1907 Ostertagia antipini Matschulski, 1950 O. leptospicularis Assadov, 1953 O. kolchida Popova, 1937 Spiculopteragia boehmi Gebauer, 1932 S. mathevossiani Ruchljadev, 1948. S. asymmetrica (Ware, 1925) Trichostrongylus askivali Dunn, 1964 Ashworthius sidemi Schulz, 1933 Aonchotheca bilobata (Bhalerao, 1933) Bovidae, number of host species Babesia divergens (M’Fadyean and Stockman, 1911) Fasciola hepatica Linnaeus, 1758 (Rudolphi, 1819) Dictyocaulus viviparus (Bloch, 1782) Ostertagia ostertagi (Stiles, 1892) O. trifurcata Ransom, 1907 Trichostrongylus axei (Cobbold, 1879) Trichuris ovis (Abildgaard, 1795) The parasitic fauna of Bison bonasus 375

Caprinae, number of host species Ostertagia circumcincta (Stadelmann, 1894) Trichostrongylus vitrinus Looss, 1905 pulchrum Molin, 1857 Psoroptes ovis (Hering, 1898)

Canidae, number of host species Neospora caninum Dubey, Carpenter, Speer, Topper and Uggla, 1988 Pallas, 1766

Polyxenic parasites Giardia spp. Toxoplasma gondii (Nicolle and Manceaux, 1908) Cryptosporidium spp. Chorioptes bovis (Hering, 1845) Ixodes ricinus Linnaeus, 1758 Dermacentor reticulatus Fabricius, 1794 Lipoptena cervi Linnaeus, 1758 sites of elk, Alces alces – Parafasciolopsis fasciolaemorpha, possible only in zoological garden conditions. For example, Nematodirella alcidis, Mazamastrongylus dagestanicus and the presence of five species of nematodes found in captive- Trichostrongylus capricola. They are noticed as new parasites breeding bison – Dictyocaulus viviparus, Nematodirus filicollis, of B. bonasus after the restoration of the elk population in east- N. spathiger, Ostertagia circumcincta, Thelazia rhodesi – ern Poland; perchance they were recorded as very rare para- as well as two , needs confirmation. sites before. Another group are the polyxenic parasites, characterised The changes in the parasite fauna of the European bison, by their wide range of hosts. These include the intestinal and during and after restitution tissue protozoan parasites and ectoparasitic able to infect a number of host species. To this group can be also in- The first descriptions of the parasite fauna of European bison cluded Taenia hydatigera, found in bison’s tissues in its larval originate from the beginning of the twentieth century (Wrób- form. This group is not numerous – their are 4 protozoa, lewski 1927). Eighteen species of parasites were recorded in 1 tapeworm and 4 arthropods, however, the prevalence and in- total, all typical for domestic , apart from two spe- tensity of infection with these species can be relatively high cific for bison (B. sedecimdecembrii and T. wrublewskii) (Fig. 2). (Wróblewski 1927). The most common parasites at this time Some records of parasite infections seems to be the result were F. hepatica, D. viviparus and D. filaria, the prevalence of of incorrect identification, or infection with a strange parasite infection with these parasites reaching 100%. The subdomi-

Fig. 2. The structure of parasite fauna of European bison Bison bonasus, in relation to the main parasite’s host and host specificity. The parasites species needed confirmation and single recorded are not mentioned 376 Grzegorz Karbowiak et al.

nant parasites were D. dendriticum, P. cervi, Moniezia ces- were S. asymmetrica and C. surnabada. Moreover, parasites todes and G. pulchrum. Moreover, some unidentified and less typical for Cervidae are still noted: P. fasciolaemorpha, numerous parasite species were also mentioned. The massive T. capricola, O. leptospicularis, O. kolchida, S. mathevossiani, infections with parasites typical for cattle were probably as- C. pectinata, N. roscidus, N. europaeus and N. alcidis. Simul- sociated with the ubiquitous herds of cattle in forests and mid- taneously, some species of helminths, previously common, dle forest . This fact is able to explain the presence stay rare, and have even not been recorded during the last few of a mite species characteristic for (P. equi) and insects years, such as H. placei (Dróżdż et al. 1994). typical for cattle and (Haematopinus eurysternus, The changes observed are not only in the species compo- ) in European bison (Wróblewski 1927, sition of parasite fauna of European bison, but also in preva- Dróżdż 2000, Demiaszkiewicz and Pyziel 2010). lence and intensity of infection. In the last few decades higher The disappearance of free-living populations of European intensities than were previously observed are the case for Fas- bison in 1919 and the survival of only a few individuals in ciola hepatica, O. ostertagii, O. leptospicularis, O. kolchida, zoological gardens and private farms possibly affected the par- N. roscidus, N. helvetianus, C. bilobata, D. viviparus and asite fauna of this animal. It is possible that parasites specific O. lienalis (Dróżdż et al. 1994; Demiaszkiewicz et al. 2008). for B. bonasus perished due to the low number of hosts, the A decrease of invasion prevalence is observed in the case of S. lack of vectors and treatment of bison with antiparasitic drugs. labiatopapillosa (Demiaszkiewicz et al. 2007). The summary At this time the typical cattle parasites – F. hepatica, Moniezia trends of changes in parasite community structure is shown in spp., Dictyocaulus spp., and G. pulchrum were not recorded or the Table II. found rarely as infestation with ectoparasites obtained from Studying the parasite fauna changes is possible only for livestock herds in the forest disappeared. Alternatively, the the helminths, with reports over almost 100 years, and for close localisation of the bison to other Bovidae and Cervidae some easily noticeable ectoparasites, such as B. sedecimde- species provided on opportunity for the transfer of new para- cembrii. Unfortunately, it is impossible to establish the sites and pathogens. Such a new nematode is A. bilobata, changes in the fauna of protozoan parasites, due to their inci- parasite of asiatic Bovidae species (Demiaszkiewicz and dental study, or because of long pauses in the monitoring, as Pyziel 2010). in the case of T. wrublewskii. After the restitution of the species, an epidemiological, bac- Parasitic arthropods and protozoa have only been studied teriological and parasitological studies began in the 1950s, in- since 1992, and there are no possibilities to establish long- cludings on the helminth fauna of animals living in captive term trends. Predominant ectoparasites are I. ricinus, D. biso- breeding reserves before they were released. The cattle para- nianus and B. sedecimdecembrii prior to last two decades, sites – F. hepatica, Moniezia spp. – were still rare; however, there were only sporadic, single observations and reports of other parasites typical for domesticated ruminants were noted – the parasites from free-ranging animals and from zoological B. trigonocephalum, T. axei, O. ostertagii, O. lyrata, S. boehmi, gardens (Izdebska 2001 b). Similar to the helminths acquired C. surnabada, N. helvetianus, T. gulosa, and T. skrjabini (Demi- from deer and elk, and the parasitising mite P. equi, the aszkiewicz and Pyziel 2010). The study followed bison after parasites were probably transferred from the appropriate host the release in open areas and was repeated after 20 years to bison, facilitated by the close emplacement of these hosts in (Dróżdż et al. 1989, 1994) and has been conducted from this the dwelling reserve in Białowieża. This same mechanism time up to the present. Since the 1980s, when the free-ranging explains the infestation with H. eurysternus, lice typical for bison population fluctuated above 250 individuals, there cattle; Wróblewski (1927) reported their presence in the Eu- appeared helminth species typical for Cervidae – P. fasciolae- ropean bison, and according to his observation, the source of morpha, T. capricola, O. leptospicularis, O. kolchida, those ectoparasites was cattle in the forest. Simulta- S. boehmi, S. mathevossiani, C. pectinata, N. roscidus, N. eu- neously, with the disappearance of the free-ranging bison from ropaeus, and N. alcidis. The predominant species were O. lep- natural forests, these parasites also became extinct from the tospicularis and N. roscidus (Dróżdż et al. 1989, 1994, host. After the reintroduction of bison to Białowieża Forest in Demiaszkiewicz and Pyziel 2010). the second half of the twentieth century, the custom of cattle During this entire period the parasite fauna didn’t change. grazing in the forest was strongly limited; consequently, there The highest prevalences were observed for gastrointestinal ne- is no possibility to transit from cattle to bison, and this louse matodes, Trichostrongylidae and C. bilobata; these are the is not recorded now. This can also be the reason to explain the most common parasites of free-ranging bison. They have at- disappearance of some parasites specific to other hosts, such tained high prevalence, which is often 100%, and high inten- as P. equi and M.ovinus, which were possibly transmitted to sity of infection. However, no pathological symptoms have bisons from livestock pastured in the forest. been observed due to the infections (Dróżdż et al. 1989). In the The trypanosomes were studied only at the beginning of following years, the predominance of gastrointestinal nema- 20th century (Wróblewski 1927), and the studies was only re- todes was also observed but the composition of nematodes peated after 70 years (Kingston et al. 1992). The investiga- was enriched by parasites typical for Cervidae. New species tions of other protozoan parasites began only during recent found to infect bison in the last decade of the twentieth century years (Osińska and Piusiński 1997; Karbowiak et al. 2004; The parasitic fauna of Bison bonasus 377

Table II. The most important changes in the parasite fauna of European bison in Białowieża Primeval Forest during XX and XXI centuries

The important circumstances Year The phenomena in parasite fauna the domination of typical cattle parasites; the presence of ectoparasites purchased of livestock the last wild-living bison shot 1919 the breeding of single specimens in various zoological the possible disappearance of the parasite species or strains gardens specific for B. bonasus; the absence of the most typical cattle parasites; the purchasing of Asiatic nematode A. bilobata; the beginning of B. bonasus restitution in Białowieża 1929 the reserve breeding and the creation of a free-ranging 1952 the dominance of parasites typical for various Bovidae population in Białowieża Forest 1959 the increase of free-ranging individuals infection with F. hepatica the stabilisation of free-ranging population size 1970–1980 new parasites purchased from sp. and C. (200–250 specimens) the restitution of A. alces in Białowieża Forest 1999–2000 the first infection with A. sidemi in Białowieża the growth of free-ranging population 2001 the first infections with nematodes purchased from A. alces 2004 the prevalence of infection with A. sidemi reaches 100% 2005 the detection of antibodies against N. caninum the free-ranging population reaches 400 individuals 2010 the decrease of the infection prevalence with some Trichostrongylidae species; the direct evidence of N. caninum

Cabaj et al. 2005; Paziewska et al. 2007; Majewska et al. imals, no pathological symptoms have been recorded (Cabaj 2010; Pyziel and Demiaszkiewicz 2009 a,b). Thus, it is im- et al. 2008, 2009, 2010). possible to verify the taxonomic status of trypanosomes stud- ied by Wrublewski (1908, 1912) and to compare them with The factors that formed the parasite fauna of B.bonasus the parasites isolated now. The early reports indicate different biological features and different pathogenicity to those ob- The natural parasitic fauna of the European bison probably al- served in more recent years. Trypanosomes found by most perished along with the demise of the natural host pop- Wrublewski at the beginning of 20th century were numerous in ulations. The European bison perhaps lost most of its natural the blood and caused serious disease of bison, similar to sleep- parasites during the period of its breeding in captivity (Dróżdż ing sickness and possibly lethal. The currently observed in- et al. 1989, 1994; Izdebska 2003). On the other hand, there tensity of infection with T. wrublewskii is low, never higher have been many opportunities for bison to be infected by par- than 50–100 individuals in 1 ml of blood, and no pathological asites from other . Therefore, the present composi- symptoms of infections are observed (Karbowiak et al. 2006). tion of parasite fauna inhabiting this host has a compound A new and very important protozoan parasite of B. bona- origin because some bison parasites presumably switched to sus is Neospora caninum . It is an obligate intracellular pro- this host during their period of breeding in captivity. The Eu- tozoan parasite, detected and described for the first time in ropean bison appears to be a new host for P. fasciolaemorpha, in Norway (Dubey et al. 1988). The definitive hosts are T. capricola, O. leptospicularis, O. kolchida, S. mathevossiani, canine (, ), however, the parasite has also been de- C. pectinata, N. roscidus, N. europaeus and N. alcidis (Dróżdż tected in the range of intermediate hosts – livestock and com- et al. 1989, 1994). The most spectacular example of such a panion animal species. For the first time, the presence of this parasite is A. sidemi. This nematode originates from , and parasite in Poland was serologically confirmed in aborted with their definitive host – sika deer (Cervus nippon) was cows in 2000 (Cabaj et al. 2000). The antibodies to N. can- transferred to Europe. It colonised the European deer species inum in European bison were reported in 2005, in 7.3% of the Cervus elaphus and from deer it was transmitted to Bison animals examined (Cabaj et al. 2005). The first direct record bonasus. In Poland, it was recorded for the first time in the of the presence of this protozoan in European bison was noted bisons population in the Bieszczady Mountains in 1997 in in 2010 (Bień et al. 2010). The prevalence of infection of Eu- 4 specimens, and over several years colonised every animals. ropean bison is different in various years; serological ELISA A similar situation was repeated later in the Białowieża tests show the prevalence ranging from 7% (years 2007–2009) Primeval Forests from 1999, when the first infections were to 13.4% (year 2009). It is evident that there has been a up- noted, to 2004 when every bison was infected (Dróżdż et al. ward trend in the prevalence level; however, in wild living an- 2003; Demiaszkiewicz et al. 2009; Demiaszkiewicz and 378 Grzegorz Karbowiak et al.

Pyziel 2010). The sources of the parasites were local red deer, currence is waekly linked the occurrence area of B. bonaus. which brought the parasite from neighbouring and Such an example is I. persulcatus, which is spread to the east (Dróżdż et al. 1998, 2002). of the main living area of Bison bonasus (Siuda 1993). Their A special case involves parasites typical for elk, recorded parasitisation of European bison is possible in principle; how- in high numbers or for the first time during the recent decades ever, it is improbable due to the different geographical areas. (Dróżdż et al. 1989, 1994, 2003; Demiaszkiewicz and Pyziel These reports need confirmation in the future. 2010). This occurrence can be associated with two processes – the restitution of B. bonasus in Białowieża Primeval Forests, Conclusions and simultaneously with the reintroduction of elk (A. alces) to this same terrain, after their absence during the first half of In summary, it can be stated that with the process of the resti- the 20th century. The elks were returned in the 1970s to tution of European bison to the natural environment, the Bialowieża Primeval Forest and met with free-living bison process of recovery and formation of parasitic fauna associ- (Pucek and Raczyński 1983). Thus, the possibility for the par- ated with this host has simultaneously taken place. The pres- asite exchange between the mammals was made. ent state is different in comparison to the parasite species It is noted that the helminth and arthropods fauna of free- richness observed before the twentieth century and to the state ranging bison is richer than those from captive reserves, due at the time of release of the first individuals from the captive to the acquisition of new species of parasites from Cervidae reserve in Białowieża Primeval Forest, and will likely con- (Dróżdż et al. 2002). tinue to change in the future. The state described in this review is the picture of the pres- ent knowledge. It is sure that it will change in the future, ac- cordive to finding new parasite species, and the verification Acknowledgements. Data unpublished earlier were obtained in of previous findings. There are also natural changes in the par- MNISW grant no N308 234738 and NCN grant no. N N308 563840. asite fauna, such as the assimilation of new parasites and the loss of previously occurring species. Such an example are Eimeria protozoan. To date there have been eleven species of References Eimeria recorded in B. bonaus (Pyziel and Demiaszkiewicz 2009 b; Pyziel et al. 2011; Pyziel unpublished), however, be- Bień J., Moskwa B., Cabaj W. 2010. In vitro isolation and identifi- cation of the first Neospora caninum isolate from European fore 2009, there was no knowledge about the presence of these bison (Bison bonasus bonasus L.). Veterinary Parasitology, parasites in European bison. Similarly, the genera Toxoplasma, 173, 200–205. DOI: 10.1016/j.vetpar.2010.06.038. Cryptosporidium and Giardia have been recorded once only Cabaj W., Bień J., Goździk K., Moskwa B. 2009. Neospora caninum or even indirectly using molecular methods (Paziewska et al. u żubrów w Polsce – aktualny stan badań. European bison 2007; Majewska et al. 2010) and we can suspect that future conservation: newsletter, 2, 102–111. Cabaj W., Bień J., Goździk K., Moskwa B. 2010. Neospora caninum studies can improve the list of parasites. u żubrów żyjących w Białowieży. European bison conserva- A additional difficulty in summarising the list of parasites tion: newsletter, 3, 63–68. associated with B. bonasus is the close similarity of many par- Cabaj W., Choromański L., Rodgers S., Moskwa B., Malczewski A. asites, and as a consequence, it is not possible to verify old 2000. Neospora caninum infections in aborting dairy cows in records. For example, Wróblewski (1927) described a high Poland. Acta Parasitologica, 45, 113–114. Cabaj W., Goździk K., Bień J., Moskwa B. 2008. Neospora caninum prevalence of infection with cestodes; however, the identifi- u żubrów – świadomość problemu. European bison conser- cation of detected species is not possible to verify now. Some vation: newsletter, 1, 53–64. species are verified and redescribed now, such as protozoa Cabaj W., Moskwa B., Pastusiak K., Gill J. 2005. Antibodies to from the Sarcocystis , and the mite D. bisonianus Neospora caninum in the blood of European bison (Bison (Kadulski and Izdebska 1996). Also, the differentiation of bonasus bonasus L.) living in Poland. Veterinary Parasitol- ogy, 128, 163–168. DOI: 10.1016/j.vetpar.2004.09.033. some closely related and morphologically similar species is Demiaszkiewicz A.W., Lachowicz J., Karbowiak G. 2007. Wzrost za- presently uncertain, such as T. wrublewskii and T. theileri, and rażenia żubrów w Puszczy Białowieskiej nicieniami Setaria identification needs to be verified using modern molecular labiatopapillosa. Wiadomości Parazytologiczne, 53, 335–338. techniques (Karbowiak et al. 2007). Similarly, molecular Demiaszkiewicz A.W., Lachowicz J., Osińska B. 2009. Nowe ogni- study can be useful in the case of the parasities identified to the sko aswortiozy dzikich przeżuwaczy w Puszczy Białowie- skiej. Magazyn Weterynaryjny, 18, 355–357. genera level only, such as Moniezia spp. (Demiaszkiewicz et Demiaszkiewicz A.W., Pyziel A.M. 2010. Forming of European al. 2008) and Demodex spp. (Izdebska 2006). By this same bison helminthfauna in Białowieża Forest. In: (Eds R. reason, it is not possible to designate which new-recorded in- Kowalczyk, D. Ławreszuk, and J.M. Wójcik) Ochrona żubra fections are, in fact, newly acquired, or are permanent, but not w Puszczy Białowieskiej. Zagrożenia i perspektywy rozwoju parasitaemias that were previously studied. populacji. ZBS PAN, Białowieża, 63–74. Demiaszkiewicz A.W., Pyziel A.M., Lachowicz J. 2008. Stan zara- The next areas of doubt are the single reports of some par- żenia żubrów helmintami w Puszczy Białowieskiej w sezo- asitic infections typical for quite different hosts, such as P. ovis nie zimowym 2007/2008. European bison conservation: and S. scabiei (Izdebska 2001 a,b) or the parasites of which oc- newsletter, 1, 42–52. The parasitic fauna of Bison bonasus 379

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