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Cestode diversity in shrews from islands in the Sea of Japan and the Sea of Okhotsk

Published online by Cambridge University Press:  03 June 2024

S.A. Kornienko*
Affiliation:
Institute of Systematics and Ecology of Animals, Siberian Branch of the Russian Academy of Sciences, Frunze Str. 11, Novosibirsk 630091, Russia
N.E. Dokuchaev
Affiliation:
Institute of Biological Problems of the North, Far East Branch of the Russian Academy of Sciences, Portovaya Str. 18, Magadan 685000, Russia
*
Corresponding author: S.A. Kornienko; Email: swetlanak66@mail.ru

Abstract

A comparative analysis of taxonomic diversity on shrew cestodes among four islands in the Sea of Japan and the Sea of Okhotsk (Sakhalin, Kunashir, Hokkaido, and Moneron) was performed. Cestode species shared among the islands were identified and their host specificity was investigated. On Sakhalin Island, 33 species of the families Hymenolepididae, Dilepididae and Mesocestoididae were recorded in four shrew species (Sorex caecutiens, S. gracillimus, S. minutissimus and S. unguiculatus). In S. caecutiens, S. gracillimus, and S. unguiculatus on Kunashir Island, 22 species of the same families were found and, on Hokkaido Island, 23 species of the families Hymenolepididae and Dilepididae were recorded. On Moneron Island, three species of cestodes were registered in S. tundrensis. The Sakhalin–Hokkaido–Kunashir complex of shrew cestodes includes eastern-Palearctic, trans-Palearctic and endemic species. High endemism (~22%) of shrew tapeworms in the Sakhalin–Kunashir–Hokkaido Islands was noted as compared to continental territories. The different numbers of cestode species in S. unguiculatus (31), S. caecutiens (29), S. gracillimus (19) and S. minutissimus (1) were found. It was concluded that the cestodes species diversity of shrews of Sakhalin–Kunashir–Hokkaido depended primarily on the history of island formation, their modern physical and geographical features, the abundance of definitive and intermediate cestodes hosts and, to a lesser extent, on the size and remoteness of the islands from the mainland and the diversity of host species.

Type
Research Paper
Copyright
© The Author(s), 2024. Published by Cambridge University Press

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References

Binkienė, R, Kornienko, SA and Tkach, VV (2015) Soricinia genovi n. sp. from Neomys fodiens in Bulgaria, with redescription of Soricinia globosa (Baer, 1931) (Cyclophyllidea: Hymenolepididae). Parasitology Research 114, 209218. DOI: 10.1007/s00436-014-4180-6CrossRefGoogle Scholar
Bogatov, VV, Pietsch, TW, Zhuravlev, YuN, Storozhenko, SY, Lelej, AS, Barkalov, VY, Kholin, SK and Prozorova, LA (2003) Origin patterns of the terrestrial and freshwater biota of the Kuril archipelago. The Bulletin of the North-East Scientific Center of FEB RAS 3, 918. [In Russian.]Google Scholar
Bogatov, VV, Pietsch, TW, Storozhenko, SY, Barkalov, VY, Lelej, AS, Kholin, SK, Krestov, PV, Kostenko, VA, Makarchenko, EA, Prozorova, LA and Shedko, SV (2006) Origin patterns of the terrestrial and freshwater biota of the Sakhalin Island. The Bulletin of the North-East Scientific Center of FEB RAS 2, 3247. [In Russian.]Google Scholar
Bugmyrin, S (2014) Calodium (Capillaria) hepaticum (Nematoda, Capillariidae) in insular small rodent populations. Principy Ekologii 4, 1830. [In Russian.]Google Scholar
Czaplinski, B and Vaucher, C (1994) Family Hymenolepididae Ariola, 1899. In Khalil, LF, Jones, A and Bray, RA (eds), Keys to the cestode parasites of vertebrates. Wallingford, UK: CAB International. pp. 595663.Google Scholar
Dokuchaev, NE (2005) “Rule of six” for the forming of multispecies communities in shrews Sorex. In Proceedings of the Ninth International Mammalogical Congress (IMC 9): Roles of Mammalogy on Coexistence of Wild Mammals and Human. Sapporo, Hokkaido University, 6970.Google Scholar
Goüy de Bellocq, J, Sarà, M, Casanova, JC, Feliu, C and Morand, S (2003). A comparison of the structure of helminth communities in the woodmouse, Apodemus sylvaticus, on islands of the western Mediterranean and continental Europe. Parasitology Research 90, 6470. DOI 10.1007/s00436-002-0806-1CrossRefGoogle Scholar
Grigoryev, EM and Bashilov, SV (1988) On the distribution of the Siberian Shrew (Sorex minutissimus Zimm., 1780) in the Kunashir Island. The Bulletin of Moscow Society of Naturalists. Biological Series 93, 7173. [In Russian.]Google Scholar
Gulyaev, VD, Kornienko, SA and Dokuchaev, NE (2007) The cestodes of the genus Staphylocystoides Yamaguti, 1959 (Cestoda, Hymenolepididae) in shrews of Beringia. The Bulletin of the North-East Scientific Center of FEB RAS 4: 7584. [In Russian.]Google Scholar
Gulyaev, VD, Zubova, OA, Dokuchaev, NE and Ohdachi, SD (2009) Revised description of Ecrinolepis ezoensis (Sawada et Koyasu, 1995) comb. n. (Cestoda, Cyclophyllidea, Ditestolepidini) in shrews from Hokkaido, Japan. The Bulletin of the North-East Scientific Center of FEB RAS 4: 5457. [In Russian.]Google Scholar
Karpenko, SV (1984) The new species of hymenolepidids (Cestoda) from the shrews of Transbaikalye. In Cherepanov, AI (Ed.), Chlenistonogie I gel’minty. Novosibirsk, Nauka, pp. 107117. [In Russian.]Google Scholar
Karpenko, SV (1997) Helminths of shrews on Kunashir Island. In Fedorov, KF (Ed.), Parasites and diseases caused by them in Siberia. Novosibirsk, Publishing house of the Siberian Branch of the Russian Academy of Agricultural Sciences, 5354. [In Russian.]Google Scholar
Karpenko, SV (1998) Helminths of shrews from sub mountain region of Western Altai. In Volkov, FA and Marchenko, VA (eds), Parasites in natural complexes and disturbed situations. Novosibirsk, Publishing house of the Siberian Branch of the Russian Academy of Agricultural Sciences, 6971. [In Russian.]Google Scholar
Karpenko, SV (1999) Cestodes of the genus Soricinia (Cyclophyllidea, Hymenolepidini) from Holarctic region shrews. Zoologicheskiy Zhurnal 78, 922928. [In Russian.]Google Scholar
Karpenko, SV (2004) Helminths of shrews of the Khabarovsk Kray. Natural resources of the Khabarovsk Kray: problems of science and education. Khabarovsk, 8086. [In Russian.]Google Scholar
Karpenko, SV and Chechulin, АI (2000) Redescription of Spalania crassisaccata (Cestoda, Cyclophyllidae, Hymenolepididae) from shrews of Kunashir Island. Zoologicheskiy Zhurnal 79, 11471154. [In Russian.]Google Scholar
Kornienko, SA and Dokuchaev, (2023) Cestode diversity of shrews on the Kamchatka Peninsula and Paramushir Island. Diversity 15, 99. DOI:10.3390/d15010099CrossRefGoogle Scholar
Kornienko, SA and Gulyaev, VD (2011) New cestodes of the genus Neoskrjabinolepis (Cestoda, Hymenolepididae) from shrews of the Far East. Zoologicheskiy Zhurnal 90, 12961303. [In Russian.]Google Scholar
Kornienko, SA, Binkienė, R and Tkach, VV (2016) Revision of the genus Soricinia Spassky & Spasskaja, 1954 (Cestoda: Cyclophyllidea: Hymenolepididae) with redescriptions of three species, an amended generic diagnosis and an identification key to species. Systematic Parasitology 93, 451465. DOI: 10.1007/s11230-016-9639-7CrossRefGoogle Scholar
Kornienko, SA, Dokuchaev, NE and Odnokurtsev, VA (2018) Shrew’ cestodes of the Central and Southern Yakutia. Zoologicheskiy Zhurnal 97, 11101120. [In Russian.] DOI: 10.1134/S0044513418090076Google Scholar
Kornienko, SA, Gulyaev, VD and Melnikova, YA (2006) On the morphology and systematics of cestodes of the genus Neoskrjabinolepis Spassky, 1947 (Cyclophyllidea, Hymenolepididae). Zoologicheskiy Zhurnal 85, 134145. [In Russian.]Google Scholar
Kornienko, SA, Gulyaev, VD and Melnikova, YA (2007) New species of cestodes of the genus Neoskrjabinolepis Spassky, 1947 (Cyclophyllidea, Hymenolepididae) from shrews of Russia. Zoologicheskiy Zhurnal 86, 259269. [In Russian.]Google Scholar
Kornienko, SA, Makarikov, A and Dokuchaev, NE (2014) Cestodes of small mammals in Bolshoy Shantar island (sea of Okhotsk western part). Bulletin of the North-East Scientific Center, FE Branch RAS 2, 6569. [In Russian.]Google Scholar
Kornienko, SA, Makarikova, ТА and Dokuchaev, (2023) Neoskrjabinolepis paradoxa n. sp. from shrews on Sakhalin Island, Russia, with an amended diagnosis of Neoskrjabinolepis Spassky, 1947 (Cestoda: Cyclophyllidea: Hymenolepididae), a key and a review on geographical distribution of the species. Journal of Helminthology 97 DOI: 10.1017/S0022149X23000524CrossRefGoogle Scholar
Kornienko, SA, Binkienė, R, Dokuchaev, NE and Tkach, VV (2019) Molecular phylogeny and systematics of cestodes with rudimentary rostellum (Cestoda: Hymenolepididae) from Holarctic Sorex shews (Eulipotyphla: Soricidae). Zoological Journal of the Linnean Society 187, 965986. DOI:10.1093/zoolinnean/zlz061CrossRefGoogle Scholar
Kornienko, SA, Gulyaev, VD, Melnikova, YA and Georgiev, BB (2008a) Neoskrjabinolepis nuda n. sp. from shrews in Sakhalin Island, Russia, with a taxonomic review of Neoskrjabinolepis Spassky, 1947 (Cyclophyllidea, Hymenolepididae). Systematic Parasitology 70, 147158.CrossRefGoogle Scholar
Kornienko, SA, Zubova, OA, Gulyaev, VD and Dokuchaev, NE (2008b) Cestodes of shrews from Kunashir Island. In Galaktionov, KV and Dobrovolskij, AA (eds), Parasitology in XXI century – problems, methods, solutions. St. Petersburg, Lema, 265268 [In Russian.]Google Scholar
Kostenko, VA and Nesterenko, VA (2006) Mammals (Mammalia) of the Moneron Island. pp. 306313. In Storozhenko, SYu (Ed) The Flora and fauna of Moneron Island (Materials of International Sakhalin Island Project) Vladivostok, Dalnauka. [In Russian.]Google Scholar
Kostenko, VA, Nesterenko, VA and Trukhin, AM (2004) Mammals of the Kuril Archipelago. Vladivostok, Dalnauka, 186 p. [In Russian.]Google Scholar
Loktionova, EYu, Nesterenko, VA and Burkovsky, ОА (2016) Dominance structure in taxocaenoses of Northern Sakhalin shrews. The Bulletin of the North-East Scientific Center of FEB RAS 2, 9399. [In Russian.]Google Scholar
Lykova, KA, Gulyaev, VD, Melnikova, YA and Karpenko, SV (2006) Diorchilepis, a new genus of cestodes (Cyclophyllidea, Hymenolepididae, Ditestolepidini) and redescription of Diorchilepis ezoensis comb. n. from shrews of Sakhalin Island and the Kuril Islands. Zoologicheskiy Zhurnal 85, 15061510. [In Russian.]Google Scholar
Lykova, КА, Melnikova, YA and Karpenko, SV (2005) Spasskylepis tiunovi sp.n. (Cyclophyllidea, Hymenolepididae) – a new cestode species from shrews of the Far East. Parasitologiya 39, 285292. [In Russian.]Google ScholarPubMed
MacArthur, RH and Wilson, EO (1967) The Theory of Island Biogeography. Princeton: Princeton Univ. Press. 293 p.Google Scholar
Magurran, (1988) Ecological Diversity and Its Measurements. Princeton: Princeton University Press. 179p.CrossRefGoogle Scholar
Mas-Coma, S and Feliu, C (1984) Helminthofauna from small mammals (insectivores and rodents) on the Pityusic islands. In Kuhbier, J, Alcover, JA and Guerau d’Arellano, C (eds), Biogeography and ecology of the Pityusic Islands. Junk, Barcelona, pp. 469525.CrossRefGoogle Scholar
Melnikova, YA and Gulyaev, VD (2004) A new cestode species – Monocercus dokuchaevi sp. nov. (Cyclophyllidea: Dilepididae) from shrews in Northeastern Asia. Parazitologiya 78, 6873. [In Russian.]Google Scholar
Melnikova, YA, Gulyaev, VD and Dokuchaev, NE (2003) The structure of community of cestodes of shrews of West Beringia and the Far East. In Alekseev, AN (Ed.), Problems of modern parasitology. St. Petersburg, Lema, 1820. [In Russian.]Google Scholar
Melnikova, YA, Gulyaev, VD and Dokuchaev, NE (2005) Cestoda of insectivorous mammals of Russian Far East. In Scientific investigations of nature in Lazovsky Reserve. Vladivostok, Russkiy Ostrov, 8290. [In Russian.]Google Scholar
Millien-Parra, V and Jaeger, JJ (1999) Island biogeography of the Japanese terrestrial mammal assemblages: an example of a relict fauna. Journal of Biogeography 26, 959972. DOI: 10.1046/j.1365-2699.1999.00346.xCrossRefGoogle Scholar
Miquel, J, Fons, R, Feliu, C, Marchand, B, Torres, J and Clara, JP (1996) Helminthes parasites des rongeurs Muridés des îles d’Hyères (Var, France): aspects écologiques. Vie Milieu 46, pp. 219223.Google Scholar
Neov, B, Vasileva, GP, Radoslavov, G, Hristov, P, Littlewood, DTJ and Georgiev, BB (2019) Phylogeny of hymenolepidid cestodes (Cestoda: Cyclophyllidea) from mammalian hosts based on partial 28S rDNA, with focus on parasites from shrews. Parasitology Research 118, 7388. DOI: 10.1007/s00436-018-6117-yCrossRefGoogle ScholarPubMed
Neov, B, Vasileva, GP, Radoslavov, G, Hristov, P, Littlewood, DTJ and Georgiev, BB (2021) Phylogeny of hymenolepidids (Cestoda: Cyclophyllidea) from mammals: Sequences of 18S rDNA and COI genes confirm major clades revealed by the 28S rDNA analyses. Journal of Helminthology 95(E23). DOI: 10.1017/S0022149X21000110CrossRefGoogle Scholar
Nesterenko, VA (1999) Insectivores of the south Far East and their communities. Vladivostok, Dalnauka. 173p. [In Russian.]Google Scholar
Nesterenko, VA, Loktionova, EYu and Burkovsky, ОА (2016) Dinamics of shrew taxocene structure in southern of Sakhalin. Contemporary Problems of Ecology 3, 333342. [In Russian.] DOI: 10.15372/SEJ20160305Google Scholar
Ochotina, MV (1976) New form of shrew (Insectivora) from Moneron Island. Zoologicheskiy Zhurnal 55, 590595. [In Russian.]Google Scholar
Ochotina, MV (1977) Shrews (Insectivora, Soricidae) from Sakhalin Island. Zoologicheskiy Zhurnal 56, 243249. [In Russian.]Google Scholar
Odnokurtsev, VA and Karpenko, SV (1993) Structure of the helminth fauna of shrews in Yakutia. In Fauna, ecology and practical significance of phyto- and zooparasitic organisms. Kishinev, Shtiintsa, pp. 6576. [In Russian.]Google Scholar
Ohdachi, SD, Ishibashi, Y, Iwasa, MA, Fukui, D and Saitoh, T (eds). (2015) The Wild Mammals of Japan. Second edition. Kyoto: Shoukadoh Book Sellers. 511 p.Google Scholar
Pietsch, TW, Bogatov, VV, Amaoka, K, Zhuravlev, YN, Barkalov, VY, Gage, S, Takahashi, H, Lele, AS, Storozhenko, SY and Minakawa, N (2003) Biodiversity and biogeography of the islands of the Kuril Archipelago. Journal of Biogeography 30, 12971310. DOI: 10.1046/j.1365-2699.2003.00956.xCrossRefGoogle Scholar
Poulin, R (1998) Comparison of three estimators of species richness in parasite component communities. Journal of Parasitology 84, 485490.CrossRefGoogle ScholarPubMed
Sato, H, Kamiya, H and Ohbayashi, M (1988) Hymenolepidid and dilepidid cestodes with armed rostellum in shrews, Sorex spp. from Hokkaido, Japan. Japanese Journal of Veterinary Research 36, 119131.Google ScholarPubMed
Sawada, I (1999) A Checklist of Cestode species from Asian Insectivora. Journal of Industrial Economics 13, 109123.Google Scholar
Sawada, I and Asakawa, M (1992) Helminth fauna of shrews on Teuri To, Rishiri To and Rebun To in Hokkaido, Japan. Bulletin of Nara Sangyo University 8, 165170.Google Scholar
Sawada, I and Harada, M (1990) Cestodes of field micromammalians (Insectivora) from central Honshu, Japan. Zoological Science 7, 469475.Google Scholar
Sawada, I and Kaneno, S (1992) Hymenolepis magnirostellata sp. n. (Cestoda: Hymenolepididae) with records of the known Cestodes from the shrews of Hokkaido. Japanese Journal of Parasitology 41, 283286.Google Scholar
Sawada, I and Kobayashi, S (1993) Cestode Parasites of Shrews in South Saghalien. Proceedings of the Japanese Society of Systematic Zoology 49, 15.Google Scholar
Sawada, I and Koyasu, K (1990) Further studies on Cestodes from Japanese shrews. Bulletin of Nara Sangyo University 6, 187202.Google Scholar
Sawada, I and Koyasu, K (1991) Cestodes of some Micromammalians (Insectivora) from Hokkaido, Japan. Japanese Journal of Parasitology 40, 567575.Google Scholar
Sawada, I and Koyasu, K (1995) Helminth Sinuterilepis ezoensis sp. nov. (Cestoda: Hymenolepididae) parasitic on Sorex caecutiens saevus from Hokkaido, Japan. Bulletin of the Biogeographical Society of Japan 50, 1517.Google Scholar
Spassky, AA (1954) Classification of hymenolepidids of mammals. Trudy Gel’mintologicheskoi Laboratorii 7, 120167. [In Russian.]Google Scholar
Spassky, AA and Andrejko, OF (1970) Cestodes of insectivora of Moldavia. Parazity Zhivotnykh i Rastenii 5, 4459. [In Russian.]Google Scholar
Vaucher, K (1992) Revision of the genus Vampirolepis Spasskij, 1954 (Cestoda: Hymenolepididae). Memórias do Instituto Oswaldo Cruz 81(1), 299304. DOI: 10.1590/S0074-02761992000500056CrossRefGoogle Scholar
Velizhanin, AG (1976) Time of isolation of the North Pacific mainland islands. Proceedings of the USSR Academy of Sciences 231(1), 205207. [In Russian.]Google Scholar
Voronov, GA, Zagorodskih, EE and Perminov, LE (1969) Shrews Sorex of Northern Sakhalin. Scientific Notes of the Perm State Pedagogical Institute. Perm 79, 6574. [In Russian.]Google Scholar
Zubova, OA, Gulyaev, VD and Kornienko, SA (2010) Soricinia sawadai sp. n. (Cyclophyllidea: Hymenolepididae), a new cestode species from the shrews of Sakhalin Island. Parasitologiya 44, 232239. [In Russian.]Google Scholar
Zubova, ОA, Kornienko, , Gulyaev, VD and Dokuchaev, NE (2008a) Cestodes of the shrews of the Sakhalin Island. In Galaktionov, KV and Dobrovolskij, AA (eds), Parasitology in XXI century – problems, methods, solutions. St. Petersburg: Lema, 265268. [In Russian.]Google Scholar
Zubova, ОA, Kornienko, , Gulyaev, VD and Dokuchaev, NE (2008b) Cestodes of the shrews of the Hokkaido (Japan). In Movsessian, SO, Be′er, SA, Zinovieva, SV, Pelgunov, AN and Spiridonov, SE (eds), Biodiversity and ecology of parasites of terrestrial and water cenoses. Moscow, Publishing house of the Russian Agricultural Academy, 135138. [In Russian.]Google Scholar