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 (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, Poland
Abstract During the last century the recorded parasite fauna of Bison bonasus includes 88 species. These are 22 species of protozoa, 4 trematode species, 4 cestode species, 43 nematode species, 7 mites, 4 Ixodidae ticks, 1 Mallophaga species, 1 Anoplura, and 2 Hippoboscidae flies. There are few monoxenous parasites, the majority of parasites are typical for other Bovidae 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 (captive breeding or free-ranging) and the possibility of contact with other ruminant 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 European bison, their pathogenicity and potential implications for conservation.
Keywords Bison bonasus, parasite
Introduction The European bison (Bison bonasus) is the largest herbivorous animal in Europe. Due to their dramatic history, their present population is composed of closely related individuals, a fact that affects the health and immunity of these animals (Kita and Anusz 2006; Krasińska and Krasiński 2007). Threats to the health of bison include viral, bacterial and parasitic diseases. The first investigations into parasites of European bison were conducted during the early twentieth century. In early years, when the European bison were present only in the captive reserves, only fragmentary studies based on small amounts of material originating from single dissections were conducted; however, the number of known parasite species reached at this time 37 (Dróżdż 1961, 1967). After the restitution of the species, an epidemiological, bacteriological and parasitological study began in the 1950’s, including study of helminth fauna of animals living in captive breeding reserves before they were released. This study followed bison after
their release into the wild, was repeated after 20 years (Dróżdż et al. 1989, 1994), and is still being conducted. Summarising the publications available, the parasite fauna of European bison is quite well described; however, most reports of parasites in B. bonasus are based on small numbers of bison from isolated single populations or zoological gardens. Therefore, the prevalence, geographical distribution and clinical significance of most parasites cannot be widely interpreted. The full list of all B. bonasus parasites is presented in the first part of the review; part 2 describes phenomena occurring in the whole parasitic fauna of B. bonasus – changes of the parasite fauna after the species reintroduction to the wild and aquisition of new parasite species. The purpose of this publication is to describe the present knowledge of the parasite fauna of the European bison B. bonasus, based on the publications of various scientific centres that have conducted parasitological studies on this animal, includes on those living in free-ranging populations as well as bred in zoological gardens and captived reserves.
*Corresponding author:
[email protected]
The parasitic fauna of Bison bonasus
The analysis of the parasite fauna and their changes during recent decades was conducted on the basis of the available literature data as well as our own observations. The diversity and structure of B. bonasus parasite fauna On the basis of publications describing parasitological studies made in the natural environment, as well as those describing cases of infections in captive-breeding European bison, it is possible to establish a list of parasites associated with the animal, and the changes in the parasite fauna from the beginning of the twentieth century, across the critical beginning of restitution, to the current state of a stable free-living population of bison at the beginning of the twenty-first century. The full list of taxa and parasite species is presented in the first part of the publication (Karbowiak et al. 2014). In summary, during the past 100 years there have been 88 species of parasites found, more or less associated with European bison. The most numerous group are the nematodes – 43 species, followed by protozoa – 22 species (Fig. 1). Almost all parasites are polyxenic, have a large range of hosts, or are shared with other wild ungulates or cattle (Kita and Anusz 2006; Krasińska and Krasiński 2007). Only 3 species parasitising B. bonasus are monoxenous parasites of this host: Trypanosoma wrublewskii, Bisonicola sedecimdecembrii and Demodex bisonianus (Table I). Currently the most common parasites of B. bonasus are nematodes belong to the Trichostrongylidae family – these are C. oncophora, O. leptospicularis, Ostertagia kolchida, O. ostertagii, and S. boehmi, for which the prevalence level reaches 90–100%. They are followed by Trichuris ovis and the fluke
373
Fasciola hepatica, recorded in 43 to 100% of bison. Also Ixodidae ticks are common parasites, found in almost every free-living bison. Other parasites are subdominant, found in up to 20% of bisons studied, with prevalence levels up to 1–3% of population. In view of the hosts preferences, the most common parasite group observed in bison are the parasites shared with cattle – these include the apicomplexan parasites from the genera Sarcocystis and Eimeria, a single species of fluke, tapeworm and mite, and 14 species of nematodes. The group of parasites that infect a range of Bovidae species, among them species having the preference for Caprinae, include 9 species of helminths, the protozoan parasite Babesia bovis and the mite Psoroptes ovis. All these species can be typical parasites of B. bonasus due to the close relationship of bison to cattle and other Bovidae. The next group are parasites specific for Cervidae. These include 17 species, including one fluke and 16 species of nematodes. Some of these species may possibly be parasites primarily shared with cervidae, however, most of them are new species received from deer. Parafasciolopsis fasciolaemorpha, Trichostrongylus capricola, Ostertagia leptospicularis, Ostertagia kolchida, Spiculopteragia mathevossiani, Cooperia pectinata, Nematodirus europaeus and Nematodirus roscidus were aquired by bison from deer during the second part of twentieth century (Dróżdż et al. 1989), while the nematode Spiculopteragia asymmetrica was recorded in bison for the first time in 1992 (Dróżdż et al. 1994). This phenomena can be related to the increase of red and roe deer numbers in Białowieża forest and contact of the restituted population of 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 Bison bonasus specific parasites
Parasite 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 Dicrocoelium dendriticum (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 Gongylonema pulchrum Molin, 1857 Psoroptes ovis (Hering, 1898)
Canidae, number of host species
Neospora caninum Dubey, Carpenter, Speer, Topper and Uggla, 1988 Taenia hydatigena 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, Nematodirella alcidis, Mazamastrongylus dagestanicus and Trichostrongylus capricola. They are noticed as new parasites of B. bonasus after the restoration of the elk population in eastern Poland; perchance they were recorded as very rare parasites before. Another group are the polyxenic parasites, characterised by their wide range of hosts. These include the intestinal and tissue protozoan parasites and ectoparasitic arthropods able to infect a number of host species. To this group can be also included Taenia hydatigera, found in bison’s tissues in its larval form. This group is not numerous – their are 4 protozoa, 1 tapeworm and 4 arthropods, however, the prevalence and intensity of infection with these species can be relatively high (Fig. 2). Some records of parasite infections seems to be the result of incorrect identification, or infection with a strange parasite
possible only in zoological garden conditions. For example, the presence of five species of nematodes found in captivebreeding bison – Dictyocaulus viviparus, Nematodirus filicollis, N. spathiger, Ostertagia circumcincta, Thelazia rhodesi – as well as two insects, needs confirmation. The changes in the parasite fauna of the European bison, during and after restitution The first descriptions of the parasite fauna of European bison originate from the beginning of the twentieth century (Wróblewski 1927). Eighteen species of parasites were recorded in total, all typical for domestic ruminants, apart from two specific for bison (B. sedecimdecembrii and T. wrublewskii) (Wróblewski 1927). The most common parasites at this time were F. hepatica, D. viviparus and D. filaria, the prevalence of 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
nant parasites were D. dendriticum, P. cervi, Moniezia cestodes and G. pulchrum. Moreover, some unidentified and less numerous parasite species were also mentioned. The massive infections with parasites typical for cattle were probably associated with the ubiquitous herds of cattle in forests and middle forest grasslands. This fact is able to explain the presence of a mite species characteristic for horses (P. equi) and insects typical for cattle and sheep (Haematopinus eurysternus, Melophagus ovinus) in European bison (Wróblewski 1927, Dróżdż 2000, Demiaszkiewicz and Pyziel 2010). The disappearance of free-living populations of European bison in 1919 and the survival of only a few individuals in zoological gardens and private farms possibly affected the parasite fauna of this animal. It is possible that parasites specific for B. bonasus perished due to the low number of hosts, the lack of vectors and treatment of bison with antiparasitic drugs. At this time the typical cattle parasites – F. hepatica, Moniezia spp., Dictyocaulus spp., and G. pulchrum were not recorded or found rarely as infestation with ectoparasites obtained from livestock herds in the forest disappeared. Alternatively, the close localisation of the bison to other Bovidae and Cervidae species provided on opportunity for the transfer of new parasites and pathogens. Such a new nematode is A. bilobata, parasite of asiatic Bovidae species (Demiaszkiewicz and Pyziel 2010). After the restitution of the species, an epidemiological, bacteriological and parasitological studies began in the 1950s, includings on the helminth fauna of animals living in captive breeding reserves before they were released. The cattle parasites – F. hepatica, Moniezia spp. – were still rare; however, other parasites typical for domesticated ruminants were noted – B. trigonocephalum, T. axei, O. ostertagii, O. lyrata, S. boehmi, C. surnabada, N. helvetianus, T. gulosa, and T. skrjabini (Demiaszkiewicz and Pyziel 2010). The study followed bison after the release in open areas and was repeated after 20 years (Dróżdż et al. 1989, 1994) and has been conducted from this time up to the present. Since the 1980s, when the free-ranging bison population fluctuated above 250 individuals, there appeared helminth species typical for Cervidae – P. fasciolaemorpha, T. capricola, O. leptospicularis, O. kolchida, S. boehmi, S. mathevossiani, C. pectinata, N. roscidus, N. europaeus, and N. alcidis. The predominant species were O. leptospicularis and N. roscidus (Dróżdż et al. 1989, 1994, Demiaszkiewicz and Pyziel 2010). During this entire period the parasite fauna didn’t change. The highest prevalences were observed for gastrointestinal nematodes, Trichostrongylidae and C. bilobata; these are the most common parasites of free-ranging bison. They have attained high prevalence, which is often 100%, and high intensity of infection. However, no pathological symptoms have been observed due to the infections (Dróżdż et al. 1989). In the following years, the predominance of gastrointestinal nematodes was also observed but the composition of nematodes was enriched by parasites typical for Cervidae. New species found to infect bison in the last decade of the twentieth century
Grzegorz Karbowiak et al.
were S. asymmetrica and C. surnabada. Moreover, parasites typical for Cervidae are still noted: P. fasciolaemorpha, T. capricola, O. leptospicularis, O. kolchida, S. mathevossiani, C. pectinata, N. roscidus, N. europaeus and N. alcidis. Simultaneously, some species of helminths, previously common, stay rare, and have even not been recorded during the last few years, such as H. placei (Dróżdż et al. 1994). The changes observed are not only in the species composition of parasite fauna of European bison, but also in prevalence and intensity of infection. In the last few decades higher intensities than were previously observed are the case for Fasciola hepatica, O. ostertagii, O. leptospicularis, O. kolchida, N. roscidus, N. helvetianus, C. bilobata, D. viviparus and O. lienalis (Dróżdż et al. 1994; Demiaszkiewicz et al. 2008). A decrease of invasion prevalence is observed in the case of S. labiatopapillosa (Demiaszkiewicz et al. 2007). The summary trends of changes in parasite community structure is shown in the Table II. Studying the parasite fauna changes is possible only for the helminths, with reports over almost 100 years, and for some easily noticeable ectoparasites, such as B. sedecimdecembrii. Unfortunately, it is impossible to establish the changes in the fauna of protozoan parasites, due to their incidental study, or because of long pauses in the monitoring, as in the case of T. wrublewskii. Parasitic arthropods and protozoa have only been studied since 1992, and there are no possibilities to establish longterm trends. Predominant ectoparasites are I. ricinus, D. bisonianus and B. sedecimdecembrii prior to last two decades, there were only sporadic, single observations and reports of the parasites from free-ranging animals and from zoological gardens (Izdebska 2001 b). Similar to the helminths acquired from deer and elk, and the horse parasitising mite P. equi, the parasites were probably transferred from the appropriate host to bison, facilitated by the close emplacement of these hosts in the dwelling reserve in Białowieża. This same mechanism explains the infestation with H. eurysternus, lice typical for cattle; Wróblewski (1927) reported their presence in the European bison, and according to his observation, the source of those ectoparasites was cattle grazing in the forest. Simultaneously, with the disappearance of the free-ranging bison from natural forests, these parasites also became extinct from the host. After the reintroduction of bison to Białowieża Forest in the second half of the twentieth century, the custom of cattle grazing in the forest was strongly limited; consequently, there is no possibility to transit from cattle to bison, and this louse is not recorded now. This can also be the reason to explain the disappearance of some parasites specific to other hosts, such as P. equi and M.ovinus, which were possibly transmitted to bisons from livestock pastured in the forest. The trypanosomes were studied only at the beginning of 20th century (Wróblewski 1927), and the studies was only repeated after 70 years (Kingston et al. 1992). The investigations of other protozoan parasites began only during recent 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 last wild-living bison shot
1919
the breeding of single specimens in various zoological gardens
The phenomena in parasite fauna the domination of typical cattle parasites; the presence of ectoparasites purchased of livestock the possible disappearance of the parasite species or strains 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 population in Białowieża Forest
1952
the dominance of parasites typical for various Bovidae
1959
the increase of free-ranging individuals infection with F. hepatica
the stabilisation of free-ranging population size (200–250 specimens) the restitution of A. alces in Białowieża Forest the growth of free-ranging population
the free-ranging population reaches 400 individuals
1970–1980
new parasites purchased from Cervus sp. and C. capreolus
1999–2000
the first infection with A. sidemi in Białowieża
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
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. 2010; Pyziel and Demiaszkiewicz 2009 a,b). Thus, it is impossible to verify the taxonomic status of trypanosomes studied by Wrublewski (1908, 1912) and to compare them with the parasites isolated now. The early reports indicate different biological features and different pathogenicity to those observed in more recent years. Trypanosomes found by Wrublewski at the beginning of 20th century were numerous in the blood and caused serious disease of bison, similar to sleeping sickness and possibly lethal. The currently observed intensity of infection with T. wrublewskii is low, never higher than 50–100 individuals in 1 ml of blood, and no pathological symptoms of infections are observed (Karbowiak et al. 2006). A new and very important protozoan parasite of B. bonasus is Neospora caninum . It is an obligate intracellular protozoan parasite, detected and described for the first time in dogs in Norway (Dubey et al. 1988). The definitive hosts are canine (dog, coyote), however, the parasite has also been detected in the range of intermediate hosts – livestock and companion animal species. For the first time, the presence of this parasite in Poland was serologically confirmed in aborted cows in 2000 (Cabaj et al. 2000). The antibodies to N. caninum in European bison were reported in 2005, in 7.3% of the animals examined (Cabaj et al. 2005). The first direct record of the presence of this protozoan in European bison was noted in 2010 (Bień et al. 2010). The prevalence of infection of European bison is different in various years; serological ELISA tests show the prevalence ranging from 7% (years 2007–2009) to 13.4% (year 2009). It is evident that there has been a upward trend in the prevalence level; however, in wild living an-
imals, no pathological symptoms have been recorded (Cabaj et al. 2008, 2009, 2010). The factors that formed the parasite fauna of B.bonasus The natural parasitic fauna of the European bison probably almost perished along with the demise of the natural host populations. The European bison perhaps lost most of its natural parasites during the period of its breeding in captivity (Dróżdż et al. 1989, 1994; Izdebska 2003). On the other hand, there have been many opportunities for bison to be infected by parasites from other mammals. Therefore, the present composition of parasite fauna inhabiting this host has a compound origin because some bison parasites presumably switched to this host during their period of breeding in captivity. The European bison appears to be a new host for P. fasciolaemorpha, T. capricola, O. leptospicularis, O. kolchida, S. mathevossiani, C. pectinata, N. roscidus, N. europaeus and N. alcidis (Dróżdż et al. 1989, 1994). The most spectacular example of such a parasite is A. sidemi. This nematode originates from Asia, and with their definitive host – sika deer (Cervus nippon) was transferred to Europe. It colonised the European deer species Cervus elaphus and from deer it was transmitted to Bison bonasus. In Poland, it was recorded for the first time in the bisons population in the Bieszczady Mountains in 1997 in 4 specimens, and over several years colonised every animals. A similar situation was repeated later in the Białowieża Primeval Forests from 1999, when the first infections were noted, to 2004 when every bison was infected (Dróżdż et al. 2003; Demiaszkiewicz et al. 2009; Demiaszkiewicz and
378
Pyziel 2010). The sources of the parasites were local red deer, which brought the parasite from neighbouring Ukraine and Slovakia (Dróżdż et al. 1998, 2002). A special case involves parasites typical for elk, recorded in high numbers or for the first time during the recent decades (Dróżdż et al. 1989, 1994, 2003; Demiaszkiewicz and Pyziel 2010). This occurrence can be associated with two processes – the restitution of B. bonasus in Białowieża Primeval Forests, and simultaneously with the reintroduction of elk (A. alces) to this same terrain, after their absence during the first half of the 20th century. The elks were returned in the 1970s to Bialowieża Primeval Forest and met with free-living bison (Pucek and Raczyński 1983). Thus, the possibility for the parasite exchange between the mammals was made. It is noted that the helminth and arthropods fauna of freeranging bison is richer than those from captive reserves, due to the acquisition of new species of parasites from Cervidae (Dróżdż et al. 2002). The state described in this review is the picture of the present knowledge. It is sure that it will change in the future, accordive to finding new parasite species, and the verification of previous findings. There are also natural changes in the parasite 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 Eimeria recorded in B. bonaus (Pyziel and Demiaszkiewicz 2009 b; Pyziel et al. 2011; Pyziel unpublished), however, before 2009, there was no knowledge about the presence of these parasites in European bison. Similarly, the genera Toxoplasma, Cryptosporidium and Giardia have been recorded once only or even indirectly using molecular methods (Paziewska et al. 2007; Majewska et al. 2010) and we can suspect that future studies can improve the list of parasites. A additional difficulty in summarising the list of parasites associated with B. bonasus is the close similarity of many parasites, and as a consequence, it is not possible to verify old records. For example, Wróblewski (1927) described a high prevalence of infection with cestodes; however, the identification of detected species is not possible to verify now. Some species are verified and redescribed now, such as protozoa from the Sarcocystis genus, and the mite D. bisonianus (Kadulski and Izdebska 1996). Also, the differentiation of some closely related and morphologically similar species is presently uncertain, such as T. wrublewskii and T. theileri, and identification needs to be verified using modern molecular techniques (Karbowiak et al. 2007). Similarly, molecular study can be useful in the case of the parasities identified to the genera level only, such as Moniezia spp. (Demiaszkiewicz et al. 2008) and Demodex spp. (Izdebska 2006). By this same reason, it is not possible to designate which new-recorded infections are, in fact, newly acquired, or are permanent, but not parasitaemias that were previously studied. The next areas of doubt are the single reports of some parasitic infections typical for quite different hosts, such as P. ovis and S. scabiei (Izdebska 2001 a,b) or the parasites of which oc-
Grzegorz Karbowiak et al.
currence is waekly linked the occurrence area of B. bonaus. Such an example is I. persulcatus, which is spread to the east of the main living area of Bison bonasus (Siuda 1993). Their parasitisation of European bison is possible in principle; however, it is improbable due to the different geographical areas. These reports need confirmation in the future. Conclusions In summary, it can be stated that with the process of the restitution of European bison to the natural environment, the process of recovery and formation of parasitic fauna associated with this host has simultaneously taken place. The present state is different in comparison to the parasite species richness observed before the twentieth century and to the state at the time of release of the first individuals from the captive reserve in Białowieża Primeval Forest, and will likely continue to change in the future.
Acknowledgements. Data unpublished earlier were obtained in MNISW grant no N308 234738 and NCN grant no. N N308 563840.
References Bień J., Moskwa B., Cabaj W. 2010. In vitro isolation and identification of the first Neospora caninum isolate from European bison (Bison bonasus bonasus L.). Veterinary Parasitology, 173, 200–205. DOI: 10.1016/j.vetpar.2010.06.038. Cabaj W., Bień J., Goździk K., Moskwa B. 2009. Neospora caninum u żubrów w Polsce – aktualny stan badań. European bison conservation: newsletter, 2, 102–111. Cabaj W., Bień J., Goździk K., Moskwa B. 2010. Neospora caninum u żubrów żyjących w Białowieży. European bison conservation: newsletter, 3, 63–68. Cabaj W., Choromański L., Rodgers S., Moskwa B., Malczewski A. 2000. Neospora caninum infections in aborting dairy cows in Poland. Acta Parasitologica, 45, 113–114. Cabaj W., Goździk K., Bień J., Moskwa B. 2008. Neospora caninum u żubrów – świadomość problemu. European bison conservation: newsletter, 1, 53–64. Cabaj W., Moskwa B., Pastusiak K., Gill J. 2005. Antibodies to Neospora caninum in the blood of European bison (Bison bonasus bonasus L.) living in Poland. Veterinary Parasitology, 128, 163–168. DOI: 10.1016/j.vetpar.2004.09.033. Demiaszkiewicz A.W., Lachowicz J., Karbowiak G. 2007. Wzrost zarażenia żubrów w Puszczy Białowieskiej nicieniami Setaria labiatopapillosa. Wiadomości Parazytologiczne, 53, 335–338. Demiaszkiewicz A.W., Lachowicz J., Osińska B. 2009. Nowe ognisko aswortiozy dzikich przeżuwaczy w Puszczy Białowieskiej. Magazyn Weterynaryjny, 18, 355–357. Demiaszkiewicz A.W., Pyziel A.M. 2010. Forming of European bison helminthfauna in Białowieża Forest. In: (Eds R. Kowalczyk, D. Ławreszuk, and J.M. Wójcik) Ochrona żubra w Puszczy Białowieskiej. Zagrożenia i perspektywy rozwoju populacji. ZBS PAN, Białowieża, 63–74. Demiaszkiewicz A.W., Pyziel A.M., Lachowicz J. 2008. Stan zarażenia żubrów helmintami w Puszczy Białowieskiej w sezonie zimowym 2007/2008. European bison conservation: newsletter, 1, 42–52.
The parasitic fauna of Bison bonasus
Dróżdż J. 1961. A study on helminths and helminthiases in bison, Bison bonasus (L.) in Poland. Acta Parasitologica Polonica, 9, 55–95. Dróżdż J. 1967. The state of research on the helminthofauna of the European bison. Acta Theriologica, 12, 377–384. Drożdż J. 2000. Influence of the migration of animals on formating of their parasitofauna. Medycyna Weterynaryjna, 56, 154–157. Dróżdż J., Demiaszkiewicz A.W., Lachowicz J. 1989. The helminth fauna of free-ranging European bison Bison bonasus L. Acta Parasitologica Polonica, 34, 117–124. Dróżdż J., Demiaszkiewicz A.W., Lachowicz J. 1994. The helminth fauna of free-ranging European bison, Bison bonasus (L), studied again 8 years after reduction of bison, in the Białowieża Forest. Acta Parasitologica, 39, 88–91. Dróżdż J., Demiaszkiewicz A.W., Lachowicz J. 1998. Ashworthius sidemi (Nematoda, Trichostrongylidae) a new parasite of the European bison Bison bonasus (L.) and the question of independence of A. gagarini. Acta Parasitologica, 43, 75–80. Dróżdż J., Demiaszkiewicz A.W., Lachowicz J. 2002. Exchange of gastrointestinal nematodes between roe and red deer (Cervidae) and European bison (Bovidae) in the Bieszczady Mountains (Carpathians, Poland). Acta Parasitologica, 47, 314–317. Dróżdż J., Demiaszkiewicz A.W., Lachowicz J. 2003. Expansion of the Asiatic parasite Ashworthius sidemi (Nematoda, Trichostrongylidae) in wild ruminants in Polish territory. Parasitology Research, 89, 94–97. Dubey J.P., Carpenter J.L., Speer C.A., Topper M.J., Uggla A. 1988. Newly recognized fatal protozoan disease of dogs. Journal of the American Veterinary Medical Association, 192, 1269– 1285. Izdebska J.N. 2001a. The occurrence of parasitic arthropods in two groups of European bison in the Białowieża Primeval Forest. Wiadomości Parazytologiczne, 47, 801–804. Izdebska J.N. 2001b. European bison arthropod parasites from captived Polish breeding facilities. Acta Parasitologica, 46, 135–137. Izdebska J.N. 2003. Bisonicola sedecimdecembrii (Mallophaga, Trichodectidae) pasożyt, który przetrwał? In: (Eds. A. Buczek and Cz. Błaszak). Stawonogi i żywiciele. Liber, Lublin, 105–115. Izdebska J.N. 2006. Skin mites (Acari: Demodecidae, Psoroptidae, and Sarcoptidae) of the European bison, Bison bonasus. Biological Letters, 43, 169–174. Kadulski S., Izdebska J.N. 1996. Demodex bisonianus sp. nov. (Acari, Demodicidae) a new parasite of the bison (Bison bonasus L.). Wiadomości Parazytologiczne, 42, 103–110. Karbowiak G., Demiaszkiewicz A.W., Pyziel A.M., Wita I., Moskwa B., Werszko J., Bień J., Goździk K., Lachowicz J., Cabaj W. 2014. 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. Acta Parasitologica, 59, 363–371. DOI: 10.2478/s11686-014-0252-0 Karbowiak G., Slemenda S., Pieniazek N.J., Rychlik L., Stanko M., Sinski E., Wita I., Czaplinska U. 2004. Babesiosis of wild animals in Poland. In: Proceedings of the 9th European Multicolloquium of Parasitology, 18–23 July 2004, Valencia, Spain, 451.
Received: October 2, 2013 Revised: January 13, 2014 Accepted for publication: April 2, 2014
379
Karbowiak G., Wita I., Czaplińska U. 2006. Trypanosoma (Megatrypanum) Wrublewskii, Wladimiroff et Yakimoff 1909, the pаrаsite of European bison (Bison bonasus L.). In: Dostizhenija i perspektivy razvitija sovremennoj parazitologii. Trudy 5 respublikanskoj nauchno-prakticheskoj konferentsii, 21–22 September 2006, Vitebsk, Belarus, 268–270 (In Russian). Karbowiak G., Wita I., Czaplińska U. 2007. Pleomorfism of trypanosomes occurring in Bison bonasus L. Wiadomości Parazytologiczne, 53 (suppl.), 54. Kingston N., Dróżdż J., Rutkowska M., Wita I., Maki L. 1992. Redescription of Trypanosoma (Megatrypanum) wrublewskii Wladimiroff et Yakimoff, 1909 from the European bison, Bison bonasus L., from Puszcza Białowieska (Poland). Acta Parasitologica, 37, 163–168. Kita J., Anusz K. 2006. Infectious diseases in Bison bonasus in the years 1910–1988. In (Eds J. Kita and K. Anusz.) Health threats for the European bison particularly in free-roaming populations in Poland. SGGW Publishers, Warsaw, 17–26. Krasińska M., Krasiński Z.A. (Eds.). 2007. European bison. The Nature Monograph. Mammal Research Institute PAS, Białowieża, 318 pp. Majewska A.C., Werner A., Moskwa B., Cabaj J. 2010. Prevalence of Toxoplasma gondii, Listeria monocytogenes and Brucella abortus antibodies in European bisons. In: XXII Zjazd Polskiego Towarzystwa Parazytologicznego, Puławy, 1–3 września 2010 – streszczenia. Puławy, Poland, 61. Osińska B., Piusiński W. 1997. Sarcocystosis of cardiac muscle in European bison (Bison bonasus) in Białowieża Forest. Wiadomości Parazytologiczne, 43, 393–398. Paziewska A., Bednarska M., Niewęgłowski H., Karbowiak G., Bajer A. 2007. Distribution of Cryptosporidium and Giardia spp. in selected species of protected and game mammals from North-Eastern Poland. Annals of Agricultural and Environmental Medicine, 14, 265–270. Pucek Z., Raczyński J.J. (Eds). 1983. Atlas of Polish Mammals. PWN, Warszawa, 188 pp. Pyziel A.M., Demiaszkiewicz A.W. 2009a. Sarcocystis cruzi (Protozoa: Apicomplexa: Sarcocystidae) u żubra (Bison bonasus) w Puszczy Białowieskiej. Wiadomości Parazytologiczne, 55, 31–34. Pyziel A.M., Demiaszkiewicz A.W. 2009b. Zarażenie żubrów w Puszczy Białowieskiej kokcydiami z rodzaju Eimeria. European bison conservation: newsletter, 2, 119–122. Pyziel A.M., Kowalczyk R., Demiaszkiewicz A.W. 2011. The annual cycle of shedding Eimeria oocysts by European bison (Bison bonasus) in the Bialowieza Primeval Forest, Poland. Journal of Parasitology, 97, 737–739. DOI: dx.doi.org/10.1645/GE2567.1 Siuda K. (Ed.). 1993. Kleszcze Polski (Acari: Ixodida). II. Systematyka i rozmieszczenie. PTP, Warszawa, 375 pp. Wróblewski K. (Ed). 1927. Żubr Puszczy Białowieskiej: monografia. Wydawnictwo Polskie, Poznań, 132 pp. Wrublewski K.J. (1908). Ein Trypanosoma des Wisent von Bielowesch. Centralblatt für Bakteriologie, Parasitenkunde und Infektionskrankheiten, 48, 162–164. Wrublewski K.J. (1912). Die Trypanosomose (Schlafkrankheit) der Wisente. Zeitschrift fűr Infektionskrankheiten, parasitäre Krankheiten und Hygiene der Haustiere, 12, 376–384.
