Mollov I., D. Georgiev, O. Todorov (Eds.) Faunistic diversity of the city of Plovdiv (), Volume 1 – Invertebrates Bulletin of the Natural History Museum – Plovdiv Bull. Nat. Hist. Mus. Plovdiv, 2018, Supplement 1: 1-6

Review of species of the recorded from the Region of Plovdiv City

Zlatka M. Dimitrova*, Margarita H. Marinova

Thracian University, Faculty of Agriculture, Department of Biology and Aquaculture, Student Campus, BG-6000 Stara Zagora, BULGARIA *Corresponding author: [email protected]

Abstract. A review of acanthocephalan species recorded from the region of Plovdiv City. A total of 11 species were reported: 3 from , 1 from , 6 from and 1 from ; 3 species has been identified at the generic level only. As hosts, 14 species were recorded: 2 , 6 amphibians, 5 avian and 1 mammalian species. A -parasite list is presented.

Key words: Acanthocephala, fish, amphibians, birds, mammals, Plovdiv City, review.

Introduction the survey of avian acanthocephalans Most of the studies summarised in the (DIMITROVA et al., 2000). present review aimed revealing the helminth The present review includes the parasites of amphibians (BACHVAROV, 1962; acanthocephalan species recorded from the 1968; 1972; 1986; 1987; BACHVAROV et al., Region of Plovdiv City until 2016. The species 1975), birds (VASILEV, 1962; BACHVAROV, list is arranged according to the classification 1988) and fishes (KIRIN, 2000a; b; c; 2006). proposed by AMIN (2013). In addition, data of There is only one study on the general distribution of the reported species acanthocephalans of mammals in the studied were presented. The nomenclature of the hosts region (GEORGIEV, 1970). There are no follows Fauna Europaea (DE JONG et al., 2014). investigations of the (paratenic hosts) in the Region of Plovdiv City. List of acanthocephalan species from the In addition, the primary data obtained by Region of Plovdiv City the above-mentioned studies have also been presented in review publications on the Meyer, 1931 helminth parasites from the fauna of Bulgaria. Order Gigantorhynchida Southwell & MacFie, 1925 These are the Catalogue of the helminth Family Gigantorhynchidae Hamann, 1892 parasites of amphibians in Bulgaria Genus Van Cleave, 1916 (BACHVAROV, 1977); the monograph on the helminth parasites of freshwater fishes in (1) Mediorhynchus sp. Bulgaria (KAKACHEVA-AVRAMOVA, 1983); the monograph on the helminth parasites of Recorded from small intestine of Meleagris insectivores and rodents (GENOV, 1984) and gallopavo Linnaeus, 1758 (VASILEV, 1962).

© Bull. Nat. Hist. Mus. Plovdiv Regional Natural History Museum – Plovdiv http://rnhm.org/en/ University of Plovdiv Publishing House Review of species of the phylum Acanthocephala recorded from the Region of Plovdiv City Order Oligacanthorhynchida Petrochenko, 1956 2002), as well as from the North America - Family USA (VAN CLEAVE, 1915) and South America- Southwell & MacFie, 1925 (PILATI et al., 2013) seem to be doubtful. Genus Travassos, 1917 (5) tenuirostris (Achmerov & Dombrowskaja-Achmerova, 1941) Yamaguti, (2) Macracanthorhynchus hirudinaceus 1963 (Pallas, 1781) Travassos, 1917 Recorded from small intestine of Esox Recorded from small intestine of Sus scrofa lucius Linnaeus, 1758, Squalius cephalus (= f. domestica Linnaeus, 1758 (GEORGIEV, 1970). Leuciscus cephalus) (KIRIN, 2000a; b; c; 2006). General distribution: Holarctic, Palaeotropical General distribution: Palaearctic - Europe (GENOV, 1984; KHOKHLOVA, 1986; ARAKI, 2003), (GIBSON, 2013) and Russian Far East Neotropical (Mexico) (SALGADO-MALDONADO, (PUGACHEV, 1983). 2005) and Australian (SMALES, 2003). Acanthocephalus sp. Recorded from small intestine of Triturus Class Meyer, 1931 karelinii (previously identified in Bulgaria as Order Echinorhynchida Southwell & MacFie, 1925 Triturus cristatus) (BACHVAROV, 1972). Family Cobbold, 1876 Genus Acanthocephalus Koelreuther, 1771 Family Yamaguti, 1939 Genus Monticelli, 1905 (3) Acanthocephalus anguillae (Müller, 1780) Lühe, 1911 (6) (Zoega in Recorded from small intestine of Squalius Müller, 1776) Van Cleave, 1924 cephalus (Linnaeus, 1758) (= Leuciscus cephalus Recorded from small intestine of Esox (Linnaeus, 1758)) (KIRIN, 2000 a; b; c). lucius, Squalius cephalus (= Leuciscus cephalus) General distribution: Palaearctic - Europe (KIRIN, 2000a; b, c; 2006). (GIBSON, 2013). The records from Lena River General distribution: Palaearctic: Europe (in and Ob River (PUGACHEV, 1983) as well as freshwater and estuarine fishes) (GIBSON, those from North America by PETROCHENKO 2013). (1956) and MCDONALD (1988) seem to need additional confirmation. Order Petrochenko, 1956 (4) Acanthocephalus ranae (Schrank, 1788) Family Van Cleave, 1916 Lühe, 1914) Genus Centrorhynchus Lühe, 1911 Recorded from small intestine of Triturus karelinii (Strauch, 1870) (previously identified (7) Centrorhynchus aluconis (Müller, 1780) as Triturus cristatus (Laurenti, 1768); Lühe, 1911 experimental infections), Bombina variegata Recorded from small intestine of Strix (Linnaeus, 1758), Rana dalmatina Fitzinger, aluco Linnaeus, 1758 (BACHVAROV, 1988). 1839, Rana temporaria Linnaeus, 1758, Rana General distribution: Palaearctic and ridibunda Pallas, 1771, Rana esculenta Oriental (DIMITROVA & GIBSON, 2005). Linnaeus, 1758, Asellus aquaticus (Linnaeus, (8) Centrorhynchus buteonis (Schrank, 1758) (natural and experimental infections) 1788) Kostylev, 1914 (BACHVAROV, 1962; 1968; 1986; 1987; Recorded from small intestine of Buteo BACHVAROV et al., 1975). rufinus (Cretzschmar, 1827) (BACHVAROV, 1988). General distribution: Palaearctic - Europe General distribution: Palaearctic and (GIBSON, 2013), Southwest Asia (Azerbaidjan, Oriental (DIMITROVA & GIBSON, 2005). ) (KURBANOV, 1979; AMIN et al., 2012; (9) Centrorhynchus conspectus Van Cleave YILDIRIMHAN & ÍNGEDOĞAN, 2013) and and Pratt, 1940 () (BYCHOVSKIY, 1935; Recorded from small intestine of Buteo RYZHIKOV et al., 1980). buteo (Linnaeus, 1758) (BACHVAROV, 1988). The records from East and Southeast Asia - General distribution: Holarctic and Oriental China (WANG & WANG, 1989; XIA et al., 2015) (DIMITROVA et al., 2000). The record of and Thailand (CHAIYABUTR & CHANHOME, HARTWICH (1956) from Chile seems doubtful.

2 Zlatka M. Dimitrova, Margarita H. Marinova Family Golvan, 1960 Order Urodela Genus Lühe, 1911 Family Salamandridae Triturus karelinii (Strauch) Synonym: (10) Plagiorhynchus (Plagiorhynchus) Triturus cristatus (Laurenti), pro parte odhneri Lundström, 1942 Acanthocephalus ranae (experimental Recorded from small intestine of Buteo infection) buteo (BACHVAROV, 1988). Acanthocephalus sp. General distribution: Palaearctic - Europe Order Anura (DIMITROVA, 2009; GIBSON, 2013). Family Bombinatoridae Bombina variegata (L.) Family Meyer, 1931 Acanthocephalus ranae Genus Lühe, 1911 Family Ranidae Rana dalmatina Fitzinger (11) Arhythmorhynchus longicollis (Villot, A. ranae 1875) Lühe, 1912 Rana temporaria L. Synonyms: Arhythmorhynchus invaginabilis A. ranae (von Linstow, 1902) Rana ridibunda Pallas Recorded from small intestine of Buteo A. ranae rufinus (BACHVAROV, 1988). Rana esculenta L. General distribution: Holarctic (DIMITROVA A. ranae et al., 2000) and Neotropical (Belize) (CANARIS Class Aves & KINSELLA, 2001). Order Ciconiiformes Arhythmorhynchus sp. (= Skrjabinorhynchus sp.) Family Ardeidae Recorded from small intestine of Ardea Ardea cinerea L. cinerea Linnaeus, 1758 (BACHVAROV, 1988). anatis Arhythmorhynchus sp. Genus Filicollis Lühe, 1911 Order Falconiformes Family Accipitridae (12) (Schrank, 1788) Lühe, Buteo buteo (L.) 1911 Centrorhynchus conspectus Recorded from small intestine of Ardea Plagiorhynchus (P.) odhneri cinerea (BACHVAROV, 1988). Buteo rufinus (Cretzschmar) General distribution: Palaearctic - Eurasia Centrorhynchus buteonis (DIMITROVA et al., 2000). Arhythmorhynchus longicollis Order Galliformes Host-parasite checklist Family Phasianidae Definitive hosts Meleagris gallopavo L. Class Mediorhynchus sp. Order Esociformes Order Strigiformes Family Esocidae Family Strigidae Esox lucius L. Strix aluco L. Acanthocephalus tenuirostris Centrorhynchus aluconis Pomphorhynchus laevis Class Mammalia Order Cypriniformes Order Artiodactyla Family Cyprinidae Family Squalius cephalus (L.). Synonym: Leuciscus Sus scrofa f. domestica L. cephalus (L.) Macracanthorhynchus hirudinaceus Acanthocephalus anguillae Intermediate hosts A. tenuirostris Pomphorhynchus laevis Class Crustacea Class Amphibia Order

3 Review of species of the phylum Acanthocephala recorded from the Region of Plovdiv City Family Asellidae Plovdivski Universitet “P. Hilendarski”, Asellus aquaticus (L.) Plovdiv, 54 p. (In Bulgarian). Acanthocephalus ranae (natural and BACHVAROV G. K. 1986. Helminths of experimental infection) amphibians in Bulgaria (morphology, , fauna, biology and ecology). Discussion Summary of Doctorate Thesis. P. As seen from the above survey, 11 Hilendarski University of Plovdiv, acanthocephalan species were recorded from Plovdiv, 52 p. (In Bulgarian). the region of Plovdiv City. In addition, 3 BACHVAROV G. 1987. Study of the development species has been identified at the generic level cycle of Acanthocephalus ranae (Schrank, only. Six of the acanthocephalan species are 1788) (Echinorhynchidae) – parasite on from avian hosts, 3 from fish host and 1 from the amphibians in Bulgaria. Travaux amphibians and mammals, respectively. The Scientifiques de l’Universite de Plovdiv, acanthocephalans recorded belong to 8 genera, Biologie, 25(6): 107-111. (In Bulgarian, 7 families, 4 orders and 2 classes. As definitive Russian and English Summary). hosts, 14 vertebrate species have been BACHVAROV G. 1988. Contribution to the knowledge recorded. These are 2 fish, 6 , 5 avian of acanthocephalans (Acanthocephala) of and 1 mammalian species. wild birds in Bulgaria (first report). Travaux Scientifiques de l’Universite de Plovdiv, References Biologie, 26(6): 255-262. (In Bulgarian, AMIN O. M. 2013. Classification of the Russian and English Summary). Acanthocephala. Folia Parasitologica, BACHVAROV G., P. PETROV, B. CHOCHEV 60(4): 273-305. 1975. Contribution to the knowledge of helminth fauna of anuran amphibians AMIN O. M., S. DÜŞEN, M. C. OĞUZ. 2012. Review of the helminth parasites of (Amphibia – Ecaudata) in Plovdiv Turkish anurans (Amphibia). Scientia Region. II. Travaux Scientifiques de Parasitologica, 13(1): 1-16. l’Universite de Plovdiv, Biologie, 13(4): 41-51. (In Bulgarian, Russian and ARAKI J. 2003. Acanthocephalans in Japan. English Summary). Progress of Medical Parasitology in BYCHOVSKIY B. E. 1935. Parasitic worms of Japan, 7: 147-159. amphibians in Kulyaba, Tadjikistan. Trudy BACHVAROV G. 1962. Helminth fauna of ecaudate Tadjikskoy Basy, 5: 135-149. (In Russian). amphibians in Plovdiv District. Izvestiya CANARIS A. G., J. M. KINSELLA .2001. na Tsentralnata Helmintologichna Helminth parasites in six species of Laboratoriya, 7: 103-111. (In Bulgarian, shorebirds (Charadrii) from the coast of Russian and English Summary). Belize. Memórias do Instituto Oswaldo BACHVAROV G. 1968. Ecological investigation Cruz, 96: 827-830. of the helminth fauna of the marsh frog CHAIYABUTR N., L. CHANHOME. 2002. (Rana ridibunda Pall.) from the state Parasites in snakes of Thailand. Bulletin fish-farm in Plovdiv. Nauchni Trudove of the Maryland Herpetological Society, na Visshiya Pedagogicheski Institut, 38(2): 39-49. Plovdiv, 6(2): 143-152. (In Bulgarian, DE JONG Y., M. VERBEEK, V. MICHELSEN, P. Russian and French Summary). BJØRN, W. LOS, F. STEEMAN, N. BAILLY, BACHVAROV G. 1972. Contribution to the C. BASIRE, P. CHYLARECKI, E. knowledge of helminth fauna of caudate STLOUKAL, G. HAGEDORN, F.T. amphibians (Amphibia – Caudata) in WETZEL, F. GLÖCKLER, A. KROUP A, G. Bulgaria. Nauchni Trudove na KORB, A. HOFFMANN, C. HÄUSER, A. Plovdivskiya Universitet “P. Hilendarski”, KOHLBECKER, A. MÜLLER, A. GÜNTSCH, 10(1): 163-165. (In Bulgarian, Russian and P. STOEV, L. PENEV. 2014. Fauna French Summary). Europaea - all European species BACHVAROV G. 1977. Catalogue of the helminth on the web. Biodiversity Data Journal, 2: parasites of amphibians in Bulgaria. e4034. doi: 10.3897/BDJ.2.e4034.

4 Zlatka M. Dimitrova, Margarita H. Marinova DIMITROVA Z. M. 2009. Acanthocephalans of KIRIN D. A. 2000b. Biodiversity and ecological the nominotypical subgenus of characteristics of the helminth sets of Plagiorhynchus (Plagiorhynchidae) from Leuciscus cephalus (L., 1758) from the charadriiform birds in the collection of River Mesta and the River Maritsa. In: the Natural History Museum, London, Sbornik Dokladi of the International with a key to the species of the Scientific Conference "Man, Nature, subgenus. ZooKeys, 6: 75-90. doi: Health", 3-4 November 2000, 10.3897/zookeys.6.94. Pamporovo, 1: 78-81. (In Bulgarian). DIMITROVA Z. M., B. B. GEORGIEV, T. KIRIN D. A. 2000c. Biodiversity and ecological GENOV 2000. Review of the avian assessment of the condition of acanthocephalans from Bulgaria. Acta freshwater ecosystems of the River Zoologica Bulgarica, 52(3): 3-22. Maritsa. In: Sbornik Dokldi of the DIMITROVA Z. M., D. GIBSON 2005. Some International Scientific Conference species of Centrorhynchus Lühe, 1911 "Man, Nature, Health", 3-4 November (Acanthocephala: Centrorhynchidae) 2000, Pamporovo, 1: 82-85. (In from collection of the Natural History Bulgarian). Museum, London. Systematic KIRIN D. A. 2006. Biodiversity of the helminth Parasitology, 62: 117-134. species and helminth communities of GENOV T. 1984. Helminths of insectivores and Esox lucius (L., 1758) from Maritsa River, rodents in Bulgaria. Publishing House Bulgaria. In: Science Papers of Faculty of of the Bulgarian Academy of Sciences, Science, Bucharest. The 35th Sofia, 348 p. (In Bulgarian, Russian and International Scientific Commuications English Summary). Session of the Faculty of Animal Science, GEORGIEV B. 1970. Helminths and Bucharest, Romania, 135-140. helminthoses in large -raising farms. KURBANOV M. H. 1979. Species composition 1. Report. Helminth fauna and of acanthocephalans (Acanthocephala) helminthocenosis in large pig-raising of Azerbaijan’s animals and several of farms. Veterinarnomeditsinski Naukiy, their biological features. Nauchnye 7(5): 35- 40 (In Bulgarian). Trudy Specialnova Obrazovaniya GIBSON D. I. 2013. Acanthocephala. Fauna Azerbaidzhanskoy SSR, 4: 27-30 (In Europaea version 2.6.2. Аvailable at: Russian). http://www.faunaeur.org. MCDONALD M. E. 1988. Key to HARTWICH G. 1956. Südamerikanische Acanthocephalen aus der Zoologischen Acanthocephala reported in waterfowl. Sammlung des Bayerischen Staates. Washington, D. C., Fish and Wildlife Zoologischer Anzeiger, 156: 299-308. Service, Resourse Publication 173, 45 p. PETROCHENKO V. I. 1956. Acanthocephalans KAKACHEVA-AVRAMOVA D. 1983. Helminths of freshwater fishes in Bulgaria. of domestic and wild animals. Vol. 1. Publishing House of the Bulgarian Publishing House of the Academy of Academy of Sciences, Sofia, 261 p. (In Science of the USSR, Moscow, 435 p. Bulgarian). (In Russian). PILATI C., R. M. DE QUADROS, K. A. A. KHOKHLOVA I. G. 1986. Acanthocephalans of BRANCO., M. A. ANDRADE, S. M. T. terrestrial from the fauna of MARQUES 2013. Acanthocephalus ranae USSR. Moscow, Nauka, 277 p. (In (Echinorhynchidae) infecting Rhinella Russian). icterica (Bufonidae) in Santa Catarina, KIRIN D. A. 2000a. Ecologofaunistical study of the helminthological communities of Brazil. Ciência Animal, 23(1): 3-8. Leuciscus cephalus L. from Maritsa PUGACHEV O. N. 1983. Helminths of freshwater fishes of Northeast Asia. River. Nauchni Trudove na Sayuza na Trudy Zoologicheskovo Instituta, Uchenite, Plovdiv, Seriya B, 1: 405-408. (In Bulgarian). Leningrad, 121: 90-113 (In Russian).

5 Review of species of the phylum Acanthocephala recorded from the Region of Plovdiv City

RYZHIKOV K. M., V. P. SHARPILO, N. N. The checklist of protozoan and SHEVCHENKO 1980. Helminths of acanthocephalan from frogs in China. amphibians from the fauna of USSR. Journal of Shanghai Normal Moscow (Nauka), 276 p. (In Russian). University (Natural Sciences), 44(2): SALGADO-MALDONADO G. 2005. Catálogo y 158-168 doi: 10.3969/J.ISSN.1000- directorio de autoridades para 5137.2015.02.008 (In Chinese, English helmintos parásitos. Departamento de Summary). Zoología, Instituto de Biología, YILDIRIMHAN H. S., S. ÍNGEDOĞAN 2013. Universidad Nacional Autónoma de Checklist of metazoon parasites México. Base de datos SNIB-Conabio, recorded in Anura and Urodela from proyectoK028, 134 p. Turkey. Turkish Journal of Zoology, SMALES L. R. 2003. An annotated checklist of 37(5): 562-575. doi: 10.3906/zoo-1209- the Australian Acanthocephala from 16. mammalian and hosts. Records of the South Australian Museum, 36: 59-82. Преглед на видовете от тип Acanthocephala, VAN CLEAVE H. J. 1915. Acanthocephala in съобщени от района на гр . Пловдив North American Amphibian. The Journal of Parasitology, 1(4): 175-178. ЗлаткаМ . Димитрова , МаргаритаХр . Маринова VASILEV I. 1962. Helminth fauna of the turkey (Meleagris gallopavo L.) in Bulgaria. Резюме: Представен е преглед на Izvestiya na Tsentralnata видовете акантоцефали, съобщени от Helmintologichna Laboratoriya, 7: 19- района на гр. Пловдив. Съобщени са 11 27 (In Bulgarian, Russian and English вида акантоцефали: 3 от риби, 1 от Summary). земноводни, 6 от птици и 1 от бозайници. Четиринадесет вида гръбначни животни са WANG P., Y. WANG 1989. Helminths of Rana съобщени като гостоприемници на spinosa from Fujian Province, including установените видове акантоцефалите: 2 вида the description of a new species сладководни риби, 6 вида земноводни, 5 Metangusticaecum ranae. Journal of вида птици и 1 вид бозайници. Представени Fujian Normal University (Natural са също и данни за общото Science Edition), 2: 75-81 (In Chinese, разпространение на установените видове. English Summary). Включен е списък на гостоприемниците на XIA W., B. HUANG, S. ZHU, M. QIFEI, H. акантоцефалите, установени от района на HONGYU, D. HUI, Z. QIPING 2015. гр. Пловдив.

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