Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2019-02-25
Page range: 257–272
Abstract views: 327
PDF downloaded: 5

Vampire in the darkness: a new genus and species of land leech exclusively bloodsucking cave-dwelling bats from China (Hirudinda: Arhynchobdellida: Haemadipsidae)

College of Biology and Environmental Sciences, Jishou University, Jishou 416000, China These authors contributed equally to the study
These authors contributed equally to the study Department of Biological Sciences, Eastern Illinois University, Charleston IL 61920, USA Institute of Evolutionary Ecology and Conservation Biology, Central South University of Forestry and Technology, Changsha 410004, China
College of Biology and Environmental Sciences, Jishou University, Jishou 416000, China
College of Biology and Environmental Sciences, Jishou University, Jishou 416000, China
College of Biology and Environmental Sciences, Jishou University, Jishou 416000, China
Department of Biological Sciences, Eastern Illinois University, Charleston IL 61920, USA
College of Biology and Environmental Sciences, Jishou University, Jishou 416000, China
College of Biology and Environmental Sciences, Jishou University, Jishou 416000, China
Guangdong Institute of Applied Biological Resource, Guangzhou 510000, China
College of Biology and Environmental Sciences, Jishou University, Jishou 416000, China
Mammalia Land leeches Sinospelaeobdella gen. n. Sinospelaeobdella wulingensis sp. n. DNA taxonomy Phylogeny Cave-dwelling bats

Abstract

Land leeches in the family Haemadipsidae are mostly from the humid tropical rainforest habitats and habitually take blood from the body of human and other animals. In the present study, we report a new species, Sinospelaeobdella wulingensis sp. n., from caves in the northern subtropical Wuling Mountains of central-south China that feeds blood exclusively on cave-dwelling bats. Based on morphological characteristics, COI gene sequence divergence, and phylogenetic analysis, a new genus Sinospelaeobdella gen. n. is established for the new species, to which a previously described species Haemadipsa cavatuses Yang et al., 2009 is transferred as S. cavatuses comb. n. We also provided extended discussion on phylogenetic relationship within the “Tritetrabdellinaeclade uncovered in a previous study, DNA taxonomy, morphological and behavioral adaptions, biogeography, and possible involvement of Sinospelaeobdella gen. n. in bat transmitted diseases of public concerns.

 

References

  1. Anthony, S.J., Johnson, C.K., Greig, D.J., Kramer, S., Che, X.Y., Wells, H., Hicks, A.L., Joly, D.O., Wolfe, N.D., Daszak, P., Karesh, W., Lipkin, W.I., Morse, S.S., Consortium, P., Mazet, J.A.K. & Goldstein, T. (2017) Global patterns in coronavirus diversity. Virus Evolution, 3 (1), 1–15.

    https://doi.org/10.1093/ve/vex012

    Blanchard, R. (1892) Description de la Xerobdella lecomtei. Memoires de la Societe Zoologique de France, 5, 539–553.

    Blanchard, R. (1894) Viaggio di Leonardo Fea in Birmanica e regioni vicine.—LVII. Hirudinées. Annales di Museo Civico di Storia Naturale, 24 (2), 113–118.

    Borda, E., Oceguera-figueroa, A. & Siddall, M.E. (2008) On the classification, evolution and biogeography of terrestrial haemadipsoid leeches (Hirudinida: Arhynchobdellida: Hirudiniformes). Molecular Phylogenetics and Evolution, 46, 142–154.

    https://doi.org/10.1006/mpev.1999.0639

    Borda, E. & Siddall, M.E. (2010) Insights into the evolutionary history of Indo-Pacific bloodfeeding terrestrial leeches (Hirudinida: Arhynchobdellida: Haemadipisdae). Invertebrate Systematics, 24, 456–472.

    https://doi.org/10.1016/j.ympev.2007.09.006

    Brower, A.V.Z. & DeSalle, R. (1994) Practical and theoretical considerations for choice of a DNA sequence region in insect molecular systematics, with a short review of published studies using nuclear gene regions. Annals of the Entomological Society of America, 87 (6), 702–716.

    https://doi.org/10.1093/aesa/87.6.702

    Chen, G.W., Chen, X.H., He, Z.W., Xu, R.H. & Zhu, D.M. (1998) A land leech from Henan Province and observations of its bloodsucking behavior. Chinese Journal of Zoology, 33, 47–48. [in Chinese]

    Darriba, D., Taboada, G.L., Doallo, R. & Posada, D. (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9 (8), 772.

    https://doi.org/10.1038/nmeth.2109

    Ding, L.M. (2004) Methods for collection, preservation and microscope-slide-preparation of bloodsucking leeches. Port Health Control, 9, 14–15. [in Chinese]

    Edgar, R.C. (2004a) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32 (5), 1792–1797.

    https://doi.org/10.1093/nar/gkh340

    Edgar, R.C. (2004b) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics, 5 (1), 113.

    https://doi.org/10.1186/1471-2105-5-113

    Ewers, W.H. (1974) Trypanosoma aunawa sp. n. from an insectivorous bat, Miniopterus tristris, in New Guinea, which may be transmitted by a leech. Journal of Parasitology, 60, 172–178.

    Folmer, O., Back, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3 (5), 294–299.

    Ge, X.Y., Li, J.L., Yang, X.L., Chmura, A.A., Zhu, G.J., Epstein, J.H., Mazet, J.K., Hu, B., Zhang, W., Peng, C., Zhang, Y.J., Luo, C.M., Tan, B., Wang, N., Zhu, Y., Grameri, G., Zhang, S.Y., Wang, L.F., Daszak, P. & Shi, Z.L. (2013) Isolation and characterization of a bat SARS-like coronavirus that uses the ACE2 receptor. Nature, 503 (7477), 535–538.

    https://doi.org/10.1038/nature12711

    Grube, A.E. (1866) Jahresbericht der Schlesischen Gesellschaft f ur Vaterlandische Cultur. Kaiserlich-Konigliche Zoologisch-Bota-nische Gesellschaft in Wien, 16, 173–184.

    Guan, S.M. & Gao, B. (2008) COI sequence, the DNA barcode affecting animal taxonomy and ecology [J]. Chinese Journal of Ecology, 27 (8), 1406–1412. [in Chinese]

    Guo, Y.J., Li, L. & Yang, R.J. (2010) Observation on the biological habits of Haemadipsa cavatuses. Chinese Science and Technology Education, 7, 61–63. [in Chinese]

    Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT[C]. In: Nucleic acids symposium series. 41 (41). Information Retrieval Ltd., London, c1979-c2000., pp. 95–98.

    Available from http://www.mbio.ncsu.edu/BioEdit/bioedit.html (accessed 21 January 2018)

    Jiang, S.H., Meng, Z.Y., Chen, X.Q. & Li, G.J. (2008) Application of rDNA sequence analysis in insect systematics. Entomotaxonomia, 30 (3), 225–238. [in Chinese]

    Kappes, H. (2013) Genetics and morphology of the genus Tritetrabdella (Hirudinea, Haemadipsidae) from the mountainous rain forests of Sabah, Borneo, reveal a new species with two new subspecies. Contributions to Zoology, 82 (4), 185–197.

    Kimura, M. (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16, 111–120.

    https://doi.org/10.1007/BF01731581

    Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. (2018) MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Molecular Biology and Evolution, 35 (6), 1547–1549.

    https://doi.org/10.1093/molbev/msy096

    Lai, Y.T., Nakano, T. & 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. https://doi.org/10.3897/zookeys.139.1711

    Moore, J.P. (1927) The Fauna of British India, including Ceylon and Burma. Hirudinea. London pp. 265–266.

    Moore, J.P. (1929) Leeches from Borneo with descriptions of new species. Proceedings of the Academy of Natural Sciences of Philadelphia, 81, 267–295.

    Moore, J.P. (1938) Leeches (Hirudinea) principally from the Malay Peninsula, with descriptions of new species. Bulletin of the Raffles Museum, 14, 64–80.

    Moore, J.P. (1946) Leeches (Hirudinea) from the Hawaiian Islands, and two new species from the Pacific region in the Bishop Museum Collection. Occasional Papers of Bernice P. Bishop Museum, 18 (11), 171–191.

    Moquin-Tandon, A. (1826) Monographie de la Famille des Hirudineés. Maison de Commerce, Montpellier, 120 pp.

    Morishima, K., Suzuki, T. & Aizawa, M. (2018) Characterization of 13 polymorphic microsatellite loci in the Japanese land leech. Parasitology international, 67 (1), 13–15.

    https://doi.org/10.1016/j.parint.2017.10.002

    Nakano, T. (2017) Diversity of leeches from Japan: recent progress in macrophagous and blood-feeding taxa. In: Motokawa, M. & Kajihara, H. (Eds.), Species Diversity of Animals in Japan. Springer Japan, Tokyo, pp. 319–340.
    https://doi.org/10.1007/978-4-431-56432-4_12

    Nakano, T., Jeratthitikul, E., Nguyen, T.T. & Panha, S. (2016) A new species of Tritetrabdella (Hirudinida: Hirudiniformes: Haemadipsidae) from northern Indochina. Raffles Bulletin of Zoology, 64, 105–116.

    Nakano, T. & Sung, Y.H. (2014) A new host record for Tritetrabdella taiwana (Hirudinida: Arhynchobdellida: Haemadipsidae) from the Asian painted frog Kaloula pulchra (Anura: Microhylidae) in Hong Kong, China, with a taxonomic note on T. taiwana. Comparative Parasitology, 81, 125–129.

    https://doi.org/10.1654/4667.1

    Oka, A. (1910) Synopsis der jepanischen Hirudineen, mit diagnosen der neuen speices. Annotationes Zoologicae Japonenses, 7, 165–183.

    Richardson, L.R. (1969) A contribution to the systematics of the hirudinid leeches, with description of new families, genera and species. Acta Zoologica Academiae Scientiarum Hungaricae, 15, 97–149.

    Richardson, L.R. (1971) The relationship of the terrestrial jawed sanguivorous g. Mesobdella to the neotropical hirudiniform leeches (Hirudinoidea). Proceedings of the Linnean Society of New South Wales, 95, 215–220.

    Richardson, L.R. (1974) A new troglobitic quadrannulate land-leech from Papua (Hirudinoidea: Haemadipsidae s.1.). Proceedings of the Linnean Society of New South Wales, 99, 57–68.

    Ringuelet, R.A. (1972) Nuevos taxia de hirudineos neotropicales con la redefinicion de Semiscolecidae y la descripcion de Cyclobdellidae fam. nov. y Mesobdellidae fam. nov. Physis, 31, 193–201.

    Ronquist, F., Teslenko, M., vander-Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542.

    https://doi.org/10.1093/sysbio/sys029

    Sawyer, R.T. (1986) Leech Biology and Behaviour. Clarendon Press and Oxford University Press, Oxford, 1065 pp.

    Seo, H.Y., Ye, E., Park, T., Kim, K.G., Won, S.H., Kim, B.J., Kim, H., Chae, J.S. & 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.

    Simon, C., Frati, F., Beckenbach, A., Crespi, B., Liu, H. & Flook, P. (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the entomological Society of America, 87, 651–701.
    https://doi.org/10.1093/aesa/87.6.651

    Smith, M.A., Rodrıguez, J.J., Whitfield, J.B., Deans, A.R., Janzen, D.H., Hallwachs, W. & Hebert, P.D.N. (2008) Extreme diversity of tropical parasitoid wasps exposed by iterative integration of natural history, DNA barcoding, morphology and collections. Proceedings of the National Academy of Sciences of the United States of America, 105, 12359–12364.
    https://doi.org/10.1073/pnas.0805319105

    Song, D.X., Zhang, J., Tan, E.G. & Liu, L.R. (1977) On some blood-sucking leeches from China. Acta Zoologica Sinica, 23 (01), 102–108. [in Chinese]

    Steiner, H. (2013) Biospeleological research in the Lao PDR. 16th International Congress of Speleology, 2013, 413–419. Available from: http://www.laoscaveproject.de/Reports/Volume1-2%20Bio.pdf (accessed 25 October 2018)

    Tan, E.G., Pan, X.G. & Feng, Q.Y. (1988) Two new species of land-leeches in Sichuan, China. Acta Zootaxonomica Sinica, 13 (1), 9–14. [in Chinese]

    Tan, E.G., Pan, X.G. & Feng, Q.Y. (2000) A new subspecies of Haemadipsa guangchuanensis chuandianensis from Sichuan Province, China (Haemadipsidae). Natural Science Journal of Hainan University, 18 (1), 46–49. [in Chinese]

    Tessler, M., Barrio, A., Borda, E., Rood-Goldman, R., Hill, M. & Siddall, M.E. (2016) Description of a soft–bodied invertebrate with microcomputed tomography and revision of the genus Chtonobdella (Hirudinea: Haemadipsidae). Zoologica Scripta, 45, 552–565.

    https://doi.org/10.1111/zsc.12165

    Tessler, M., Weiskopf, S.R., Berniker, L., Hersch, R., Mccarthy, K.P., Yu, D. & Siddall, M.E. (2018) Bloodlines: mammals, leeches, and conservation in southern Asia, Systematics and Biodiversity, 16 (5), 488–496.

    Vaughan, T.A., Ryan, M.J., Czaplewski, N.J. (Eds.) & Liu, Z.X. (Trans.) (2017) Mammalogy. 6th Edition. Science Press, Beijing, pp. 396–410. [in Chinese]

    Whitman, C.O. (1886) The leeches of Japan. Quarterly Journal of Microscopy Science, 26, 317–416.

    Yang, T. (1996) The fauna of Hirudinea in China. Science press, Beijing, 259 pp. [pp. 2–35 + 148–172, in Chinese]

    Yang, T., Mo, X. & Wang, D.B. (2009) A new species of cvernous blood-sucking land leech (Hirudinea, Haemadipsidae) in the west of Yunnan Province, China. Zoological Systematics, 34, 125–129. [in Chinese]

    Zhang, Y.H. & Zhu, D.H. (2012) Large karst caves distribution and development in China. Journal of Guilin University of Technology, 32 (1), 20–28. [in Chinese]

    Zhou, X., Frandsen, P.B., Holzenthal, R.W., Beet, C.R., Bennett, K.R., Blahnik, R.J., Bonada, N., Cartwright, D., Chuluunbat, S., Cocks, G.V., Collins, G.E., deWaard, J., Dean J., Flint Jr, O.S., Hausmann, A., Hendrich, L., Hess, M., Hogg, I.D., Kondratieff, B.C., Malicky, H., Milton, M.A., Morinie `re, J., Morse, J.C., Mwangi, F.N., Pauls, S.U., Gonzalez, M.R., Rinne, A, Robinson, J.L., Salokannel, J., Shackleton, M., Smith, B., Stamatakis, A., StClair, R., Thomas, J.A., Zamora-Mun˜oz, C., Ziesmann, T. & Kjer, K.M. (2016) The Trichoptera barcode initiative: a strategy for generating a species-level Tree of Life. Philosophical Transactions of the Royal Society B Biological Sciences, 371 (1702), 20160025.

    https://doi.org/10.1098/rstb.2016.0025