Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-29T09:32:23.905Z Has data issue: false hasContentIssue false
  • English
  • Français

Host–parasite relationships between seabirds and the haemadipsid leech Chtonobdella palmyrae (Annelida: Clitellata) inhabiting oceanic islands in the Pacific Ocean

Published online by Cambridge University Press:  18 September 2020

Takafumi Nakano Open the ORCID record for Takafumi Nakano [Opens in a new window] ,
Hajime Suzuki ,
Naoko Suzuki ,
Yuichi Kimura ,
Tatsuo Sato ,
Hiromi Kamigaichi ,
Naoki Tomita  and
Takeshi Yamasaki Open the ORCID record for Takeshi Yamasaki [Opens in a new window]
Takafumi Nakano*
Affiliation:
Department of Zoology, Graduate School of Science, Kyoto University, Kyoto606-8502, Japan
Hajime Suzuki
Affiliation:
Institute of Boninology, Ogasawara, Tokyo100-2101, Japan United Graduate School of Agricultural Science, Tokyo University of Agriculture and Technology, Utsunomiya, Tochigi321-8505, Japan
Naoko Suzuki
Affiliation:
Institute of Boninology, Ogasawara, Tokyo100-2101, Japan
Yuichi Kimura
Affiliation:
Japanese Bird Banding Association, Abiko, Chiba270-1145, Japan
Tatsuo Sato
Affiliation:
The Friends of the Gyōtoku Wild Bird Observatory, Ichikawa, Chiba272-0137, Japan
Hiromi Kamigaichi
Affiliation:
Ufugi Nature Museum, Ministry of the Environment, Kunigami, Okinawa905-1413, Japan
Naoki Tomita
Affiliation:
Yamashina Institute for Ornithology, Abiko, Chiba270-1145, Japan
Takeshi Yamasaki
Affiliation:
Yamashina Institute for Ornithology, Abiko, Chiba270-1145, Japan
*
Author for correspondence: Takafumi Nakano, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The duognathous haemadipsid leeches of the genus Chtonobdella show a trans-oceanic distribution throughout the Indo-Pacific region. Although passive long-distance dispersal (LDD) of Chtonobdella leeches by birds has been suggested, little is known about the host–parasite relationships between avian hosts and Chtonobdella leeches. In the current study, we investigated Chtonobdella leech infestations of the eyes and other mucus membranes of migratory procellariiform seabirds, Pterodroma hypoleuca and Oceanodroma tristrami, captured at six locations in the Bonin Islands, Honshu and Okinawa Island, Japan. Analyses of the partial sequences of 18S rRNA, 28S rRNA, and mitochondrial cytochrome c oxidase subunit I (COI) and morphological examination of the specimens demonstrated that the Chtonobdella leeches belonged to Chtonobdella palmyrae, which is indigenous to Palmyra Atoll in the Northern Line Islands. A dominant COI sequence type was observed in samples from all six sites; therefore, C. palmyrae almost surely dispersed approximately 1000 km by infesting the eyes and mucus membranes of procellariiform seabirds. The host–parasite relationships between procellariiform seabirds and C. palmyrae provide explicit evidence of the LDD of duognathous haemadipsid leeches. The taxonomic status of Haemadipsa zeylanica ivosimae from the Volcano Islands is also briefly discussed.

Keywords

Avian hostblood-feedingHaemadipsidaeHirudiniformesmigrationoverseas dispersal
Type
Research Article
Information
Parasitology , Volume 147 , Issue 14 , December 2020 , pp. 1765 - 1773
Check for updates
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aizawa, M and Morishima, K (2018) Distribution of Haemadipsa japonica in Japan before the 1980s. Journal of the Japanese Forest Society 100, 65–69.10.4005/jjfs.100.65CrossRefGoogle Scholar
Benham, WB (1909) Preliminary report on two Hirudinea from the subantarctic islands of New Zealand. In Chilton, C (ed.), The Subantarctic Islands of New Zealand. Reports on the Geo-Physics, Geology, Zoology, and Botany of the Islands Lying to the South of New Zealand, Based on Observations and Collections Made during an Expedition in the Government Steamer ‘Hinemoa’ (Captain J. Bollons) in November, 1907, Vol. 1. Wellington: Philosophical Institute of Canterbury, pp. 372–376.Google Scholar
Boles, W (2020) Eastern yellow robin (Eopsaltria australis), version 1.0. In del Hoyo, J, Elliott, A, Sargatal, J, Christie, DA and de Juana, E (eds), Birds of the World. Ithaca, NY, USA: Cornell Lab of Ornithology. https://doi.org/10.2173/bow.yelrob1.01 (Accessed 16 July 2020).Google Scholar
Borda, E (2006) A revision of the Malagabdellinae (Arhynchobdellida: Domanibdellidae), with a description of a new species, Malagabdella niarchosorum, from Ranomafana National Park, Madagascar. American Museum Novitates 3531, 1–13.10.1206/0003-0082(2006)3531[1:AROTMA]2.0.CO;2CrossRefGoogle Scholar
Borda, E and Siddall, ME (2011) Insights into the evolutionary history of Indo-Pacific bloodfeeding terrestrial leeches (Hirudinida: Arhynchobdellida: Haemadipisidae). Invertebrate Systematics 24, 456–472.CrossRefGoogle Scholar
Borda, E, Oceguera-Figueroa, A and Siddall, ME (2008) On the classification, evolution and biogeography of terrestrial haemadipsoid leeches (Hirudinida: Arhynchobdellida: Hirudiniformes). Molecular Phylogenetics and Evolution 46, 142–154.CrossRefGoogle Scholar
Chiba, H, Kawakami, K, Suzuki, H and Horikoshi, K (2007) The distribution of seabirds in the Bonin Islands, southern Japan. Journal of the Yamashina Institute for Ornithology 39, 1–17.CrossRefGoogle Scholar
Chiba, H, Sasaki, T and Horikoshi, K (2012) Rediscovery of breeding of the Bonin petrel Pterodroma hypoleuca on Kitano-Shima Island. Ogasawara Kenkyu Nenpo 35, 45–48.Google Scholar
Collar, N and Kirwan, GM (2020) Madagascar magpie-robin (Copsychus albospecularis), version 1.0. In del Hoyo, J, Elliott, A, Sargatal, J, Christie, DA and de Juana, E (eds), Birds of the World. Ithaca, NY, USA: Cornell Lab of Ornithology. https://doi.org/10.2173/bow.mamrob1.01 (Accessed 16 July 2020).Google Scholar
Collar, N, Robson, C and Schulenberg, TS (2020) Crossley's vanga (Mystacornis crossleyi), version 2.0. In Schulenberg, TS and Keeney, BK (eds), Birds of the World. Ithaca, NY, USA: Cornell Lab of Ornithology. https://doi.org/10.2173/bow.crobab1.02 (Accessed 16 July 2020).Google Scholar
Crompton, DWT (1997) Birds as habitat for parasites. In Clayton, DH and Moore, J (eds), Host–Parasite Evolution: General Principles and Avian Models. Oxford, UK: Oxford University Press, pp. 253–270.Google Scholar
Davies, RW, Govedich, FR and Moser, WE (2008) Leech parasites of birds. In Atkinson, CT, Thomas, NJ and Hunter, DB (eds), Parasitic Diseases of Wild Birds. Ames: Wiley-Blackwell, pp. 499–511.Google Scholar
Dietrich, M, Gomez-Diaz, E and McCoy, KD (2011) Worldwide distribution and diversity of seabird ticks: implications for the ecology and epidemiology of tick-borne pathogens. Vector-Borne and Zoonotic Diseases 11, 453–470.CrossRefGoogle ScholarPubMed
Eldredge, LG and Miller, SE (1997) Numbers of Hawaiian species: supplement 2, including a review of freshwater invertebrates. Bishop Museum Occasional Papers 48, 3–22.Google Scholar
Ewers, WH (1974) Trypanosoma aunawa sp. n. from an insectivorous bat, Miniopterus tristris, in New Guinea, which may be transmitted by a leech. The Journal of Parasitology 60, 172–178.CrossRefGoogle Scholar
Fahmy, M, Ravelomanantsoa, NAF, Youssef, S, Hekkala, E and Siddall, M (2019) Biological inventory of Ranomafana National Park tetrapods using leech-derived iDNA. European Journal of Wildlife Research 65, 70.10.1007/s10344-019-1305-3CrossRefGoogle Scholar
Folch, A, Christie, DA and Garcia, EFJ (2020) Emu (Dromaius novaehollandiae), version 1.0. In del Hoyo, J, Elliott, A, Sargatal, J and Christie, DA and de Juana, E (eds), Birds of the World. Ithaca, NY, USA: Cornell Lab of Ornithology. https://doi.org/10.2173/bow.emu1.01 (Accessed 16 July 2020).Google Scholar
Gillespie, RG, Baldwin, BG, Waters, JM, Fraser, CI, Nikula, R and Roderick, GK (2012) Long-distance dispersal: a framework for hypothesis testing. Trends in Ecology & Evolution 27, 47–56.CrossRefGoogle ScholarPubMed
Hoberg, EP and Brooks, DR (2010) Beyond vicariance: integrating taxon pulses, ecological fitting, and oscillation in evolution and historical biogeography. In Morand, S and Krasnov, BR (eds), The Biogeography of Host-Parasite Interactions. Oxford, UK: Oxford University Press, pp. 7–20.Google Scholar
Huang, T, Liu, Z, Gong, X, Wu, T, Liu, H, Deng, J, Zhang, Y, Peng, Q, Zhang, L and Liu, Z (2019) Vampire in the darkness: a new genus and species of land leech exclusively blood-sucking caev-dwelling bats from China (Hirudinida: Arhynchobdellida: Haemadipsidae). Zootaxa 4560, 257–272.CrossRefGoogle Scholar
Itoh, T (2003) Class Hirudinea. In Nishida, M, Shikatani, N and Shokita, S (eds), The Flora and Fauna of Inland Waters in the Ryukyu Islands. Hadano: Tokai University Press, pp. 197–202.Google Scholar
Janovy, JJ (1997) Protozoa, helminths, and arthropods of birds. In Clayton, DH and Moore, J (eds), Host–Parasite Evolution: General Principles & Avian Models. Oxford, UK: Oxford University Press, pp. 303–337.Google Scholar
Johansson, L (1924) Ein neuer Landblutegel aus den Juan Fernandez-Inseln. In Skottsberg, C (ed.), The Natural History of Juan Fernandez and Easter Island, Vol. III, Zoology. Part III. Uppsala: Almqvist & Wiksells Boktryckeri-A.-B., pp. 439–460.Google Scholar
Kang, J-G, Won, S, Kim, H-W, Kim, B-J, Park, B-K, Park, T-S, Seo, H-Y and Chae, J-S (2016) Molecular detection of Bartonella spp. in terrestrial leeches (Haemadipsa rjukjuana) feeding on human and animal blood in Gageo-do, Republic of Korea. Parasites & Vectors 9, 326.CrossRefGoogle ScholarPubMed
Katoh, K and Standley, DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772–780.10.1093/molbev/mst010CrossRefGoogle ScholarPubMed
Lai, Y-T, Nakano, T and Chen, J-H (2011) Three species of land leeches from Taiwan, Haemadipsa rjukjuana comb. n., a new record for Haemadipsa picta Moore, and an updated description of Tritetrabdella taiwana (Oka). ZooKeys 139, 1–22.Google Scholar
Lande, VMvd (1994) Haemadipsid leeches of New Guinea: a review of their biology and a guide to identification. Science in New Guinea 20, 9–22.Google Scholar
Lanfear, R, Calcott, B, Ho, SYW and Guindon, S (2012) PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29, 1695–1701.CrossRefGoogle ScholarPubMed
Lanfear, R, Frandsen, PB, Wright, AM, Senfeld, T and Calcott, B (2017) PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution 34, 772–773.Google ScholarPubMed
Langrand, O (2020) Ground-rollers (Brachypteraciidae), version 1.0. In del Hoyo, J, Elliott, A, Sargatal, J, Christie, DA and de Juana, E (eds), Birds of the World. Ithaca, NY, USA: Cornell Lab of Ornithology. https://doi.org/10.2173/bow.brachy2.01 (Accessed 16 July 2020).Google Scholar
Leigh, JW and Bryant, D (2015) POPART: full-feature software for haplotype network construction. Methods in Ecology and Evolution 6, 1110–1116.10.1111/2041-210X.12410CrossRefGoogle Scholar
Lepage, D (2020a) Checklist of the birds of Madagascar. Retrieved from Avibase, the World Bird Database website: https://avibase.bsceoc.org/checklist.jsp?lang=EN&region=mg&list=clements&format=1 (Accessed 16 July 2020).Google Scholar
Lepage, D (2020b) Checklist of the birds of Palmyra Atoll. Retrieved from Avibase, the World Bird Database website: https://avibase.bsc-eoc.org/checklist.jsp?lang=EN&region=umpa&list=howardmoore&format=1 (Accessed 16 July 2020).Google Scholar
Lill, A and Boesman, PFD (2020a) Albert's lyrebird (Menura alberti), version 1.0. In del Hoyo, J, Elliott, A, Sargatal, J, Christie, DA and de Juana, E (eds), Birds of the World. Ithaca, NY, USA: Cornell Lab of Ornithology. https://doi.org/10.2173/bow.alblyr1.01 (Accessed 16 July 2020).Google Scholar
Lill, A and Boesman, PFD (2020b) Superb lyrebird (Menura novaehollandiae), version 1.0. In del Hoyo, J, Elliott, A, Sargatal, J, Christie, DA and de Juana, E (eds), Birds of the World. Ithaca, NY, USA: Cornell Lab of Ornithology. https://doi.org/10.2173/bow.suplyr1.01 (Accessed 16 July 2020).Google Scholar
Minh, BQ, Schmidt, HA, Chernomor, O, Schrempf, D, Woodhams, MD, von Haeseler, A and Lanfear, R (2020) IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Molecular Biology and Evolution 37, 1530–1534.CrossRefGoogle ScholarPubMed
Momiyama, T (1930) On the birds of the Bonin and Iwo Islands. Bulletin of the Biogeographical Society of Japan 1, 89–186.Google Scholar
Moore, JP (1927) The segmentation (metamerism and annulation) of the Hirudinea. In Harding, WA and Moore, JP (eds), The Fauna of British India, including Ceylon and Burma, Hirudinea. London: Taylor & Francis, pp. 1–12.Google Scholar
Morishima, K and Aizawa, M (2019) Nuclear microsatellite and mitochondrial DNA analyses reveal the regional genetic structure and phylogeographical history of a sanguivorous land leech, Haemadipsa japonica, in Japan. Ecology and Evolution 9, 5392–5406.CrossRefGoogle ScholarPubMed
Nakano, T (2010) A new species of the genus Orobdella (Hirudinida: Arhynchobdellida: Gastrostomobdellidae) from Kumamoto, Japan, and a redescription of O. whitmani with the designation of the lectotype. Zoological Science 27, 880–887.CrossRefGoogle Scholar
Nakano, T (2012a) A new sexannulate species of Orobdella (Hirudinida, Arhynchobdellida, Orobdellidae) from Yakushima Island, Japan. ZooKeys 181, 79–93.10.3897/zookeys.181.2932CrossRefGoogle Scholar
Nakano, T (2012b) A new species of Orobdella (Hirudinida, Arhynchobdellida, Gastrostomobdellidae) and redescription of O. kawakatsuorum From Hokkaido, Japan with the phylogenetic position of the new species. ZooKeys 169, 9–30.CrossRefGoogle Scholar
Nakano, T (2016) Four new species of the genus Orobdella from Shikoku and Awajishima island, Japan (Hirudinida, Arhynchobdellida, Orobdellidae). Zoosystematics and Evolution 92, 79–102.10.3897/zse.91.7616CrossRefGoogle Scholar
Nakano, T (2017) Diversity of leeches from Japan: recent progress in macrophagous and blood-feeding taxa. In Motokawa, M and Kajihara, H (eds), Species Diversity of Animals in Japan. Tokyo: Springer Japan, pp. 319–340. doi: 10.1007/978-4-431-56432-4_12.CrossRefGoogle ScholarPubMed
Nakano, T and Itoh, T (2011) A list of the leech (Clitellata: Hirudinida) collection deposited in the Department of Zoology, The University Museum, The University of Tokyo. The University Museum, The University of Tokyo, Material Reports 90, 85–94.Google Scholar
Nakano, T, Jeratthitikul, E, Nguyen, TT and Panha, S (2016) A new species of Tritetrabdella (Hirudinida: Hirudiniformes: Haemadipsidae) from northern Indochina. Raffles Bulletin of Zoology 64, 105–116.Google Scholar
O'Donoghue, P (2017) Haemoprotozoa: making biological sense of molecular phylogenies. International Journal for Parasitology: Parasites and Wildlife 6, 241–256.Google ScholarPubMed
Oka, A (1930) Sur une variété de l’Haemadipsa zeylanica s'attaquant aux Oiseaux. Proceedings of the Imperial Academy 6, 82–84.CrossRefGoogle Scholar
Phillips, AJ, Oosthuizen, JH and Siddall, ME (2011) Redescription, phylogenetic placement, and taxonomic reassignment of Mesobdella lineata (Sciacchitano, 1959) (Hirudinida: Arhynchobdellida). American Museum Novitates 3711, 1–11.CrossRefGoogle Scholar
Rambaut, A, Drummond, AJ, Xie, D, Baele, G and Suchard, MA (2018) Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67, 901–904.CrossRefGoogle ScholarPubMed
Richardson, LR (1974) A new troglobitic quadrannulate land-leech from Papua (Hirudinoidea: Haemadipsidae s.l.). Proceedings of the Linnean Society of New South Wales 99, 57–68.Google Scholar
Richardson, LR (1975) A contribution to the general zoology of the land-leeches (Hirudinea: Haemadipsoidea superfam. nov.). Acta Zoologica Academiae Scientiarum Hungaricae 21, 119–152.Google Scholar
Richardson, LR (1981) On the Papuan Elocobdella novabritanniae, the Oceanian Abessebdella palmyrae (Haemadipsoidea: Domanibdellidae), and an Oceanian barbronid (Hirudinea). Records of the Australian Museum 33, 673–694.CrossRefGoogle Scholar
Richardson, LR and Hunt, P (1968) Trypanosomes in the crop of an haemadipsid leech. Australian Journal of Science 30, 374–375.Google Scholar
Ringuelet, RA (1955) Sobre la sangijuela terrestre de Juan Fernández (Philaemon skottbergii Joh., Hirunidea). Investigaciones Zoológicas Chilenas 2, 137–142.Google Scholar
Ronquist, F, Teslenko, M, van der Mark, P, Ayres, DL, Darling, A, Höhna, S, Larget, B, Liu, L, Suchard, MA and Huelsenbeck, JP (2012) Mrbayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.CrossRefGoogle ScholarPubMed
Russell, E, Rowley, I and Christie, DA (2020) Australian Magpie (Gymnorhina tibicen), version 1.0. In del Hoyo, J, Elliott, A, Sargatal, J, Christie, DA and de Juana, E (eds), Birds of the World. Ithaca, NY, USA: Cornell Lab of Ornithology. https://doi.org/10.2173/bow.ausmag2.01 (Accessed 16 July 2020).Google Scholar
Saura, S, Bodin, Ö and Fortin, M-J (2014) Stepping stones are crucial for species’ long-distance dispersal and range expansion through habitat networks. Journal of Applied Ecology 51, 171–182.CrossRefGoogle Scholar
Sawyer, RT (1986) Leech Biology and Behaviour. Oxford, UK: Clarendon Press.Google Scholar
Schnell, IB, Sollmann, R, Calvignac-Spencer, S, Siddall, ME, Yu, DW, Wilting, A and Gilbert, MTP (2015) iDNA from terrestrial haematophagous leeches as a wildlife surveying and monitoring tool – prospects, pitfalls and avenues to be developed. Frontiers in Zoology 12, 24.CrossRefGoogle ScholarPubMed
Schnell, IB, Bohmann, K, Schultze, SE, Richter, SR, Murray, DC, Sinding, M-HS, Bass, D, Cadle, JE, Campbell, MJ, Dolch, R, Edwards, DP, Gray, TNE, Hansen, T, Hoa, ANQ, Noer, CL, Heise-Pavlov, S, Sander Pedersen, AF, Ramamonjisoa, JC, Siddall, ME, Tilker, A, Traeholt, C, Wilkinson, N, Woodcock, P, Yu, DW, Bertelsen, MF, Bunce, M and Gilbert, MTP (2018) Debugging diversity – a Pan-continental exploration of the potential of terrestrial blood-feeding leeches as a vertebrate monitoring tool. Molecular Ecology Resources 18, 1282–1298.CrossRefGoogle ScholarPubMed
Seo, H-Y, Eun, Y, Park, T-S, Kim, K-G, Won, S-H, Kim, B-J, Kim, H-W, Chae, J-S and Nakano, T (2013) First report of blood-feeding terrestrial leech, Haemadipsa rjukjuana Oka, 1910 (Hirudinida: Arhynchobdellida: Haemadipsidae) in Korea. Korean Journal of Soil Zoology 17, 14–18.Google Scholar
Seto, NW and O'Daniel, DL (2020) Bonin petrel (Pterodroma hypoleuca), version 1.0. In del Hoyo, J, Elliott, A, Sargatal, J, Christie, DA and de Juana, E (eds), Birds of the World. Ithaca, NY, USA: Cornell Lab of Ornithology. https://doi.org/10.2173/bow.bonpet.01 (Accessed 16 July 2020).Google Scholar
Siddall, ME, Rood-Goldman, R, Barrio, A and Barboutis, C (2013) The eyes have it: long-distance dispersal by an intraorbital leech parasite of birds. The Journal of Parasitology 99, 1137–1139.CrossRefGoogle Scholar
Slotterback, JW (2020) Tristram's storm-petrel (Oceanodroma tristrami), version 1.0. In del Hoyo, J, Elliott, A, Sargatal, J, Christie, DA and de Juana, E (eds), Birds of the World. Ithaca, NY, USA: Cornell Lab of Ornithology. https://doi.org/10.2173/bow.trspet.01 (Accessed 16 July 2020).Google Scholar
Taylor, B (2020) White-throated rail (Dryolimnas cuvieri), version 1.0. In del Hoyo, J, Elliott, A, Sargatal, J, Christie, DA and de Juana, E (eds), Birds of the World. Ithaca, NY, USA: Cornell Lab of Ornithology. https://doi.org/10.2173/bow.whtrai1.01 (Accessed 16 July 2020).Google Scholar
Tessler, M, Barrio, A, Borda, E, Rood-Goldman, R, Hill, M and Siddall, ME (2016) Description of a soft-bodied invertebrate with microcomputed tomography and revision of the genus Chtonobdella (Hirudinea: Haemadipsidae). Zoologica Scripta 45, 552–565.10.1111/zsc.12165CrossRefGoogle Scholar
Tessler, M, de Carle, D, Voiklis, ML, Gresham, OA, Neumann, JS, Cios, S and Siddall, ME (2018a) Worms that suck: phylogenetic analysis of Hirudinea solidifies the position of Acanthobdellida and necessitates the dissolution of Rhynchobdellida. Molecular Phylogenetics and Evolution 127, 129–134.CrossRefGoogle Scholar
Tessler, M, Weiskopf, SR, Berniker, L, Hersch, R, McCarthy, KP, Yu, DW and Siddall, ME (2018b) Bloodlines: mammals, leeches, and conservation in southern Asia. Systematics and Biodiversity 16, 488–496.CrossRefGoogle Scholar
The Ornithological Society of Japan (2012) Check-list of Japanese Birds, 7th Revised Edn. Sanda: The Ornithological Society of Japan.Google Scholar
Viana, DS, Santamaria, L and Figuerola, J (2016) Migratory birds as global dispersal vectors. Trends in Ecology & Evolution 31, 763–775.10.1016/j.tree.2016.07.005CrossRefGoogle ScholarPubMed
Wilkialis, J and Davies, RW (1980) The reproductive biology of Theromyzon tessulatum (Glossiphoniidae: Hirudinoidea), with comments on Theromyzon rude. Journal of Zoology 192, 421–429.CrossRefGoogle Scholar
Yabsley, MJ (2008) Eimeria. In Atkinson, CT, Thomas, NJ and Hunter, DB (eds), Parasitic Diseases of Wild Birds. Ames: Wiley-Blackwell, pp. 162–180.Google Scholar
Supplementary material: File

Nakano et al. supplementary material

Table S1

Download Nakano et al. supplementary material(File)
File 12.7 KB