Parasitol Res DOI 10.1007/s00436-015-4420-4

ORIGINAL PAPER

Acanthocephalans of the genus Centrorhynchus (Palaeacanthocephala: Centrorhynchidae) of birds of prey (Falconiformes) and owls (Strigiformes) in Slovakia P. Komorová & M. Špakulová & Z. Hurníková & M. Uhrín

Received: 29 January 2015 / Accepted: 4 March 2015 # Springer-Verlag Berlin Heidelberg 2015

Abstract Three species of thorny-headed worms of the genus Centrorhynchus were found to parasitize birds of prey and owls in the territory of the Slovakia during the years 2012– 2014. Out of 286 examined bird individuals belonging to 23 species, only Buteo buteo, Buteo rufinus, Falco tinnunculus (Falconiformes), Asio otus, Strix aluco, Strix uralensis and Tyto alba (Strigiformes) were infected by acanthocephalans. All the bird species except for S. aluco represent new host records for Slovakia. The most prevalent acanthocephalan Centrorhynchus aluconis was detected in all 15 examined birds of non-migratory Ural owl S. uralensis (P=100 %); however, it was found occasionally also in two individuals of the tawny owl S. aluco (P=20 %), one long-eared owl A. otus (P=7.7 %), one barn owl T. alba (P=33.3 %) and the common buzzard B. buteo (P = 0.8 %). Two other thorny-headed worms occurred exclusively in Falconiformes in raw or mixed infections: Centrorhynchus buteonis was found in 11 individuals of B. buteo (P=9.2 %), and two birds (B. buteo and B. rufinus) were parasitized simultaneously by C. buteonis and the species Centrorhynchus globocaudatus. Moreover, the latest, relatively rare acanthocephalan was found alone in two common kestrels F. tinnunculus (P= 2.7 %). Regarding intensity of infection, it ranged from a single female of C. buteonis, C. globocaudatus or C. aluconis P. Komorová (*) : Z. Hurníková Department of Epizootology and Parasitology, Institute of Parasitology, The University of Veterinary Medicine and Pharmacy in Košice, Komenského 73, 041 81 Košice, Slovakia e-mail: [email protected] M. Špakulová : Z. Hurníková Institute of Parasitology, Slovak Academy of Sciences, Hlinkova 3, 040 01 Košice, Slovakia M. Uhrín Institute of Biology and Ecology, Pavol Jozef Šafárik University in Košice, Moyzesova 11, 041 54 Košice, Slovakia

per host (four cases) to a maximum of 82 C. aluconis per an Ural owl. The difference in acanthocephalan species spectrum between birds of prey and owls in Slovakia was apparent. Keywords Thorny-headed worms . Centrorhynchus . Raptors . Buteo . Falco . Asio . Strix . Tyto

Introduction Around the world, birds of prey and owls serve as final hosts of a c a n t h o c e p h a l a n s o f t h e g e n u s C e n t ro rh y n c h u s (Centrorhynchidae, Polymorphida, Palaeacanthocephala) (Amin 2013). In the territory of Slovakia, only two representatives of the genus have been reported from the bird hosts until now, namely Centrorhynchus aluconis (Müller, 1780) and Centrorhynchus globocaudatus (Zeder, 1800) by Ryšavý (1957) and Škarda (1964). Similar species spectrum was found in birds also in neighbouring countries as Hungary (Dimitrova et al. 1995), Poland (Furmaga 1957), Austria (Kutzer et al. 1982; Kritscher 1985) and Czech Republic (Tenora and Lusk 1960; Michálek 1984; Okulewicz and Sitko 2002; Sitko 1994, 2011); however, some reports on the last two regions included other congeners, Centrorhynchus buteonis (Schrank, 1788) from Austria and the Czech Republic and Centrorhynchus conspectus Van Cleave et Pratt, 1940 from the Czech Republic. The aim of this study was to obtain new data about acanthocephalans of wide spectrum of raptorial birds from whole region of Slovakia.

Material and methods In years 2012–2014, intestines of 286 birds of prey and owls from the territory of Slovakia were examined for the presence of acanthocephalans. Sixteen falconiform bird species were examined (numbers of individuals are in brackets): Buteo

Parasitol Res

buteo (L., 1758) (n=119), Falco tinnunculus L., 1758 (n=73), Accipiter nisus (L., 1758) (n=9), Aquila heliaca Savigny, 1809 (n = 6), Accipiter gentilis (L., 1758) (n = 5), Falco peregrinus Tunstall, 1771 (n=5), Buteo rufinus (Cretzschmar, 1829) (n=4), Buteo lagopus (Pontoppidan, 1763) (n=5), Circus aeruginosus (L., 1758) (n=4), Falco subbuteo L., 1758 (n=3), Falco cherrug J. E. Gray, 1834 (n=3), Milvus milvus (L., 1758) (n=1), Pernis apivorus (L., 1758) (n=1), Circus pygargus (L., 1758) (n=1), Haliaeetus albicilla (L., 1758) (n = 1) and Falco columbarius L., 1758 (n = 1). Out of Strigiformes, seven species were dissected: Strix uralensis Pallas, 1771 (n=15), Asio otus (L., 1758) (n=13), Strix aluco L., 1758 (n=10), Tyto alba (Scopoli, 1769) (n=3), Bubo bubo (L., 1758) (n=2), Athene noctua (Scopoli, 1769) (n=1) and Glaucidium passerinum (L., 1758) (n=1). As all raptorial birds and owls are strictly protected in Slovakia, the research was conducted under the special permit of the Ministry of Environment of the Slovak Republic. All the birds examined in this study died naturally or as a result of injury or disease and were frozen before the parasitological dissection. The samples came from the various locations of Slovakia and were donated by following departments of the State Nature Conservancy of the Slovak Republic—Slovenský kras National Park, Slovenský raj National Park, Pieniny National Park and Regional Conservation Centre in Prešov and Vihorlat protected area, as well as by the Museum of the Tatra National Park, the Clinic for birds and exotic animals of the University of veterinary medicine and pharmacy in Košice, Raptor protection of Slovakia, Rehabilitation station in ZOO Bojnice and Košice Airport Bioprotection. After de-freezing of the material, acanthocephalan parasites were isolated from intestines of birds during parasitological autopsy, washed in tap water and preserved in 70 % ethanol. Before species identification according to morphological characters, selected worms were cleared in glycerine or lactophenol. The species were determined using keys and papers of Meyer (1933), Petrochenko (1958), Dimitrova et al. (1997) and Dimitrova and Gibson (2005).

Results In total, six out of 23 bird species (26.1 %) and 34 out of 286 examined bird individuals (11.9 %) were infected by some of three Centrorhynchus species, namely C. aluconis, C. globocaudatus and/or C. buteonis. All but two hosts were infected by a single acanthocephalan species, and the remaining two cases represented the mixed infections by C. buteonis and C. globocaudatus (Table 1). All infected birds came from the Central and Eastern Slovakia. Regarding Falconiformes, three out of 16 examined species (18.8 %) and 15 out of 241 bird individuals (P=6.2 %) had acanthocephalans; the common buzzard B. buteo was the most often infected raptor having all three Centrorhynchus species

(Tables 1 and 2). Four out of seven owl (Strigiformes) species (57.1 %) and 19 out of 45 bird individuals (P=42.2 %) were parasitized by thorny-headed worms. The tawny owl S. aluco, the long-eared owl A. otus, the barn owl T. alba and the Ural owl S. uralensis were infected exclusively by C. aluconis, the Ural owl in 100 % prevalence (Tables 1 and 2). The intensity of infection ranged from a single female of C. buteonis, C. globocaudatus or C. aluconis per host (four cases) to a maximum of 82 specimens of C. aluconis/Ural owl (Table 2). The frequency of female worms in individual bird hosts was regularly higher than this of males, and the approximate mean sex ratio was 3 to 1. C. aluconis The most frequent acanthocephalan C. aluconis was confirmed to occur primarily in Strigiformes, being found in four (A. otus, S. aluco, S. uralensis, T. alba) out of seven examined owl species (Table 1). As mentioned above, the most common bird host of this species is apparently S. uralensis with 100 % prevalence and rather high values of intensity of infection (Table 2). Exceptionally, C. aluconis was detected also in a single representative of Falconiformes, i.e. in common buzzard B. buteo; however, all five worms were juvenile. The detailed data are summarized in Table 2. C. globocaudatus The species C. globocaudatus was exclusively confirmed in two out of 16 examined common kestrels F. tinnunculus (Table 1); however, only unfertilized females (n=1 and n=2) were present in both hosts. Additionally, both sexes of C. globocaudatus were found in mixed infections with C. buteonis in two other birds (see below). C. buteonis The last acanthocephalan species C. buteonis was exclusively found in 11 B. buteo. A maximum intensity of infection was 15 worms (11 females and four males); two birds had a single female worm without eggs. As mentioned above, common infection by C. buteonis and C. globocaudatus is presented below. C. globocaudatus and C. buteonis mixed infection One B. buteo and one long-legged buzzard B. rufinus were hosts of mixed infection by C. globocaudatus and C. buteonis (Table 1). The first host had only three C. globocaudatus (one male and two females) and two C. buteonis (one male and one female); the second bird host had three C. globocaudatus (two males and one female) and 41 C. buteonis (11 males and 30 females).

Parasitol Res Table 1

Occurrence of Centrorhynchus spp. in birds of prey and owls in Slovakia

Bird

Number of examined/ positive birds

Order/species

Number of birds infected by Centrorhynchus spp. C.aluconis

C.buteonis

C.globocaudatus

C. buteonis+ C. globocaudatus

Falconiformes Accipiter gentilis Accipiter nisus Aquila heliaca Buteo buteo Buteo lagopus Buteo rufinus Circus aeruginosus Circus pygargus

241/15 5 9 6 119/12 5 4/1 4 1

1 – – – 1 – – – –

10 – – – 10 – – – –

2 – – – – – – – –

2 – – – 1 – 1 – –

Falco columbarius Falco cherrug Falco peregrinus Falco subbuteo Falco tinnunculus Haliaeetus albicilla Milvus milvus Pernis apivorus Strigiformes Asio otus Athene noctua Bubo bubo Glaucidium passerinum Strix aluco Strix uralensis Tyto alba

1 3 5 3 73/2 1 1 1 45/19 13/1 1 2 1 10/2 15/15 3/1

– – – – – – – – 19 1 – – – 2 15 1

– – – – – – – – – – – – – – – –

– – – – 2 – – – – – – – – – – –

– – – – – – – – – – – – – – – –

Discussion In Slovakia, acanthocephalans of birds of prey and owls have not been comprehensively studied. In fact, only two records were published. Ryšavý (1957) described unspecified number of males and females of C. aluconis from one S. aluco originated from vicinity of Gabčíkovo, while Škarda (1964) reported C. globocaudatus from a single red kite M. milvus from Zemplín region. Later, those ancient data have been listed in the review of Sitko (2011). Therefore, all the recent findings represent new host or geographical records for Slovakia, except for the two hitherto mentioned cases. An apparent discrepancy in acanthocephalan species spectrum has been revealed by the present study between the birds of prey and the owls, as the latter were found to be parasitized exclusively by C. aluconis while the birds of prey had predominantly C. buteonis or C. globocaudatus alone or in mixed infections. However, ability of B. buteo to be infected by C. aluconis was also demonstrated here. The strong differences in helminth communities of owls and birds of

prey were shown also by Santoro et al. (2012) in Southern Italy. Considering majority of other literature data on acanthocephalans of raptorial birds, host specificity of individual Centrorhynchus species seems to be really low. For instance, C. aluconis seems to be more or less bound to the owl hosts in Europe (Kutzer et al. 1982; Kritscher 1985; Ewald and Crompton 1993; McInnes et al. 1994; Sitko 1994; Dimitrova et al. 1995; Ferrer et al. 2004; Dimitrova and Dimitrova 2012; Santoro et al. 2012), but it was sometimes reported also in Falconiformes (Yamaguti 1963; Illescas Gomez et al. 1993; Borgsteede et al. 2003; Sitko 2011). On the other hand, C. buteonis was mentioned predominantly as a parasite of a range of birds of prey but also the owls of the genus Strix (Furmaga 1957; Yamaguti 1963; Michálek 1984; Kritscher 1985; Sitko 2011; Dimitrova and Dimitrova 2012; Dipineto et al. 2013; Shirazi et al. 2014). The widest host spectrum has often been reported in C. globocaudatus by many of the above cited sources; however, birds of prey predominated (Sanmartín et al. 2004). A striking difference was noted between the occurrence of C. aluconis in two congeneric owl species, namely S. aluco

– – – – – – – – – – – –

a

P prevalence, II intensity of infection

Two buzzards (one B. buteo and one B. rufinus) were parasitized by mixed infection of C. buteonis and C. globocaudatus

– – – – – – – – 7.7 20 100 33.3 13/1 10/2 15/15 3/1

5 7.5 22.4 (2–82) 2

♂1/♀4 ♂2 (1–3)/♀5.5 (4–7) ♂4.9 (0–18)/♀17.5 (2–64) ♂1/♀1

– – – –

♂1/♀2 ♂3/♀2 ♂-/♀1.5 (1–3) 3 5 1.5 0.8 25.0 2.7 ♂1.7 (0–4)/♀3.7 (1–11) ♂10/♀29 – 6.4 (1–15) 39 – 9.2 25.0 – ♂2/♀3 – –

Mean II (range) males/females Mean II (range)

5 – – 0.8 – – 119/12a 4/1 73/2

Falconiformes Buteo buteo Buteo rufinus Falco tinnunculus Strigiformes Asio otus Strix aluco Strix uralensis Tyto alba

Mean II (range) males/females Mean II (range) P (%) P (%) P (%)

Mean II (range)

Centrorhynchus buteonis Centrorhynchus aluconis Number of examined/ positive birds Host birds

Table 2

Prevalence, mean intensity of infection and minimum–maximum numbers of Centrorhynchus spp. in host birds

Mean II (range) males/females

Centrorhynchus globocaudatus

Parasitol Res

and S. uralensis. Although the number of birds examined was comparable (10 and 15, respectively), the prevalence was 20 % in S. aluco while 100 % in S. uralensis. In Slovakia, both owls were reported either in sympatry or allopatry (Obuch 2011; Obuch et al. 2013) but little is known about their detailed space segregation which was demonstrated e.g. by Vrezec and Tome (2004) in Slovenia. However, variable acanthocephalan load might rather relate to differences in the diet of tawny and Ural owls, related either to allopatric localities or to a food competition in case of sympatry. It is well known that S. aluco is a very adaptable species which tolerates various forest and arable and urban environments and catches really broad spectrum of prey while larger S. uralensis is more specialized in natural, mainly forest areas and the proportion of small mammals (including moles) or reptiles in its diet is much larger (Vrezec and Tome 2004; Obuch 2011; Obuch et al. 2013). Information on mammal and reptile paratenic hosts of Centrorhynchus acanthocephalans, namely Neomys, Sorex spp., Natrix natrix and Vipera berus, is known from Central Europe (Prokopič and Mahnert 1970; Kritscher 1985; Lewin 1992; Tkach 1993; Lewin and Grabda-Kazubska 1997). Another uncommon feature concerns the mixed infection of C. buteonis and C. globocaudatus which was detected in two host birds, B. buteo and B. rufinus. In both cases, C. globocaudatus specimens were sparse but adult and both sexes were present. Regarding the intensity of infection, it ranged from a single female of C. buteonis or C. globocaudatus per host (three cases) to a maximum of 82 C. aluconis per an Ural owl. All Centrorhynchus infections without male individuals comprised unfertilized females, regardless of the species, and no case of exclusive male infection occurred. Almost always the number of the females outweighed the males, and females with copulatory caps covering the posterior body end were found predominantly in rich infections. In most papers, the Centrorhynchus sex ratio was not analysed at all. Considering the European continent, six Centrorhynchus species were listed as parasites of raptorial birds by the hostparasite database of the Natural History Museum, London (Gibson et al. 2005). In addition to C. aluconis, C. buteonis and C. globocaudatus, also the species Centrorhynchus clitorideus (Meyer, 1931), Centrorhynchus amphibius Das, 1950 and Centrorhynchus conspectus have been provided by the mentioned database (Gibson et al. 2005). However, the situation regarding the last three congeners is a little bit messy. For instance, C. clitorideus was reported only two times from the distant regions of Kaliningrad and Calabria from A. otus and A. noctua (Meyer 1933; Santoro et al. 2012), while C. amphibius was originally described as juvenile worms from Indian amphibians. Yamaguti (1963) mentioned that C. amphibius might be considered as larvae of C. clitorideus, but the adults of the first species were reported from Bulgaria

Parasitol Res

(Dimitrova et al. 1997; Dimitrova and Gibson 2005) and Turkey (Tezel et al. 2014). However, the authors recognized some variability in morphological features of the parasites from different geographical areas. Therefore, an assessment of the species status would be highly beneficial. The species C. conspectus, reported as a parasite of Otus scops from the Czech Republic (Sitko 2011) and B. buteo from Bulgaria (Dimitrova and Dimitrova 2012), was originally described (Van Cleave and Pratt 1940) and later thoroughly re-described from North American Strigiformes Strix varia, Bubo virginianus, and Otus asio, as well as from various US mammals and reptiles as paratenic hosts (Richardson and Nickol 1995). Thus, it would be very interesting to compare the American and European materials using thorough morphological and molecular approaches. Meanwhile, the whole species spectrum of the genus Centrorhynchus comprising a tremendous amount of 97 species worldwide (Amin 2013) would merit in-depth analysis like it was done in the Nearctic and Neotropical regions. Namely, Richardson and Nickol (1995) recognized only six valid Centrorhynchus species in the northern area while Lunaschi and Drago (2010) reported a key for nine Neotropical congeners. However, some papers have still reported undetermined Centrorhynchus material from America (e.g. Santos and Amato 2010; Hamann et al. 2014). Acknowledgments We are grateful to the persons, agencies and institutions that provided the material for this study, namely Milan Olekšák, Ervín Hapl, Jozef Chavko and all innominates from the State Nature Conservancy of the Slovak Republic. This work was supported by the Grant Agency of the Slovak Republic VEGA (1/0702/12 and 2/068/13).

References Amin OM (2013) Classification of Acanthocephala. Folia Parasitol 60: 273–305. doi:10.14411/fp.2013.031 Borgsteede FHM, Okulewicz A, Zoun PEF, Okulewicz J (2003) The helminth fauna of birds of prey (Accipitriformes, Falconiformes and Strigiformes) in the Netherlands. Acta Parasitol 48:200–207 Dimitrova Z, Dimitrova N (2012) Review of species of the phylum Acanthocephala from the Middle-Bulgarian Region. Agric Sci Technol Stara Zagora 4:159–165 Dimitrova ZM, Gibson DI (2005) Some species of Centrorhynchus Luhe, 1911 (Acanthocephala: Centrorhynchidae) from the collection of the Natural History Museum, London. Syst Parasitol 62:117–134. doi: 10.1007/s11230-005-5486-7 Dimitrova ZM, Murai E, Genov T (1995) Some species of the family Centrorhynchidae Van Cleave, 1916 (Acanthocephala) from Hungarian birds. Parasitol Hung 28:89–99 Dimitrova ZM, Georgiev BB, Genov T (1997) Acanthocephalans of the family Centrorhynchidae (Paleacanthocephala) from Bulgaria. Folia Parasitol 44:224–232 Dipineto L, Borrelli L, Pepe P, Fioretti A, Caputo V, Cringoli G, Rinaldi L (2013) Synanthropic birds and parasites. Avian Dis 57:756–758 Ewald JA, Crompton DWT (1993) Centrorhynchus aluconis (Acanthocephala) and other helminth species in tawny owls (Strix

aluco) in Great Britain. J Parasitol 79:952–954, Stable URL: http:// www.jstor.org/stable/3283737 Ferrer D, Molina R, Castella J, Kinsella JM (2004) Parasitic helminths in the digestive tract of six species of owls (Strigiformes) in Spain. Vet J 167:181–185. doi:10.1016/S1090-0233(03)00103-5 Furmaga S (1957) The helminth fauna of predatory birds (Accipitres and Striges) of the environment of Lublin. Acta Parasitol Pol 1957:215– 287 Gibson DI, Bray RA, Harris EA (Compilers) (2005) Host-Parasite Database of the Natural History Museum, London. URL Hamann MI, Kehr AI, González CE (2014) Helminth community structure in the Argentinean bufonid Melanophryniscus klappenbachi: importance of habitat use and season. Parasitol Res 113:3639– 3649. doi:10.1007/s00436-014-4029-z Illescas Gomez MP, Rodriguez Osorio M, Aranda Maza F (1993) Parasitation of falconiform, strigiform and passeriform (Corvidae) birds by helminths in Spain. Res Rev Parasitol 53:129–135 Kritscher E (1985) Catalogus faunae Austriae: Aschelminthes, Schlauchwürmer; Nemertini, Schnurwürmer. Teil 4. Phylum: Acanthocephala. Verlag der Österreichischen Akademie de Wissenshaften. Wien. IV d: 1–15 (in German) Kutzer E, Frey H, Nöbauer H (1982) Zur parasitenfauna österreichischer eulenvögel (Strigiformes). Angew Parasitol 23:190–197 Lewin J (1992) Parasites of the water snake, Natrix natrix L., in Poland. Acta Parasitol 37:195–199 Lewin J, Grabda-Kazubska B (1997) Parasites of Vipera berus L. in Poland. Acta Parasitol 42:92–96 Lunaschi LI, Drago FB (2010) A new species of Centrorhynchus (Acanthocephala (Centrorhynchidae) endoparasite of Guira guira (Aves, Cuculidae) from Argentina. Helminthologia 47:38–47. doi: 10.2478/s11687-010-0007-x McInnes FJ, Crompton DWT, Ewald JA (1994) The distribution of Centrorhynchus aluconis (Acanthocephala) and Porrocaecum spirale (Nematoda) in tawny owls (Strix aluco) from Great Britain. J Raptor Res 28(1):34–38 Meyer A (1933) Acanthocephala. Vierter Band, 2. Abt. 2. Academische Verlagsgesellshaft M.B.H, Buch, pp 1–582 Michálek J (1984) Physaloptera alata Rudolphi, 1819 and Centrorhynchus buteonis (Schrank, 1788) in Falconiformes in Czechoslovakia. Folia Parasitol 31:383–384 Obuch J (2011) Spatial and temporal diversity of the diet of the tawny owl (Strix aluco). Slov Raptor J 5:1–120. doi:10.2478/v10262-0120057-8 Obuch J, Danko Š, Mihók J, Karaska D, Šimák L (2013) Diet of the Ural owl (Strix uralensis) in Slovakia. Slov Raptor J 7:59–71. doi:10. 2478/srj-2013-003 Okulewicz J, Sitko J (2002) Acanthocephala of birds in the Czech Republic. Helminthologia 39:176 Petrochenko VI (1958) Acanthocephalans of domestic and wild animals, vol 2. Academy Science USSR, Moscow, 456 pp. (in Russian) Prokopič J, Mahnert V (1970) Über Helminthen der Kleinsäuger (Insectivora, Rodentia) Tirols (Österreichs). Ber Nat–Med Ver Innsbruck 58:143–154, In German Richardson DJ, Nickol BB (1995) The genus Centrorhynchus (Acanthocephala) in North America with description of Centrorhynchus robustus n. sp., redescription of Centrorhynchus conspectus, and a key to species. J Parasitol 8:767–772 Ryšavý B (1957) Zur Kenntnis der Helminthenfauna der Vögel in der Tschechoslowakei. Česk Parasitol 4:299–329, In Czech, with German summary Sanmartín ML, Álvarez F, Barreiro G, Leiro J (2004) Helminth fauna of falconiform and strigiform birds of prey in Galicia, Northwest Spain. Parasitol Res 92:255–263. doi:10.1007/s00436-003-1042-z Santoro M, Mattiucci S, Nascetti G, Kinsella JM, Di Prisco F, Sabatino T, D’Alessio N, Veneziano V, Aznar FJ (2012) Helminth communities of owls (Strigiformes) indicate strong biological and ecological

Parasitol Res differences from birds of prey (Accipitriformes and Falconiformes) in Southern Italy. PLoS ONE 7(12):e53375. doi:10.1371/journal. pone.0053375 Santos VGT, Amato SB (2010) Helminth fauna of Rhinella fernandezae (Anura: Bufonidae) from the Rio Grande do Sul Coastland, Brazil: analysis of the parasite community. J Parasitol 96:823–826. doi:10. 1645/GE-2388.1 Shirazi S, Hesaraki S, Mostafaei TS, Davoodi J (2014) First report on Centrorhynchus aluconis in common buzzard (Buteo buteo) in Northwest Iran. Acta Vet Beograd 64:276–280. doi:10.2478/acve2014-0026 Sitko J (1994) Helminths of birds of prey (Falconiformes) and owls (Strigiformes) in the Czech Republic and their influence on health condition of caged birds. Zprávy MOS 52:53–84, In Czech, with German summary Sitko J (2011) Checklist of the Acanthocephala in birds in the Czech Republic and the Slovak Republic. Comenius Museum Přerov 2011, 35 pp. IBSN 978-80-903713-8-5 Škarda J (1964) The helminth fauna of some wild birds in Czechoslovakia. Acta Univ Agric Brno B 12:269–293, In Czech, with English summary

Tenora F, Lusk S (1960) Beitrag zur näheren Erkenntnis der Helminthenfauna bei Raubvögeln (Falconiformes) in der Tschechoslowakei. Acta Univ Agric Brno A 4:205–211, In Czech, with German summary Tezel M, Girisgin AO, Birlik S, Yildirimham HS, Senlik B (2014) Helminths of the digestive tract in Buteo buteo (Falconiformes: Falconidae) in Bursa Province of Northwest Turkey. Turk J Zool 38:1–5. doi:10.3906/zoo-1403-24 Tkach VV (1993) First report on the helminths of insectivores from the Danube Delta. Analele tiin ifice ale Institutului Delta Dunării 197– 201 Van Cleave HJ, Pratt EM (1940) A new species of the genus Centrorhynchus (Acanthocephala) from the barred owl. J Parasitol 26:297–300 Vrezec A, Tome D (2004) Altitudinal segregation between Ural Owl Strix uralensis and tawny owl S. aluco: evidence for competitive exclusion in raptorial birds. Bird Study 51:264–269. doi:10.1080/ 00063650409461362 Yamaguti S (1963) Acanthocephala. Vol V Systema Helminthum. Interscience New York, 423pp