Skip to main content Skip to main navigation menu Skip to site footer
Responsive image
Issue: Vol. 5301 No. 2: 9 Jun. 2023
Type: Article
Published: 2023-06-09
DOI: 10.11646/zootaxa.5301.2.3
Page range: 199-218
Abstract views: 681
PDF downloaded: 18

Taxonomic status of the Lesser Woolly Horseshoe bats (Chiroptera, Rhinolophidae, Rhinolophus beddomei) in peninsular India and Sri Lanka

Ecology and Conservation Lab; School of Biological Sciences; University of Reading; Whiteknights; Reading; UK
Wildlife Biology and Taxonomy Lab; Department of Zoology; Osmania University; Hyderabad; Telangana State 500007; India; Systematics; Ecology and Conservation Laboratory; Zoo Outreach Organization; 96; Kumudham Nagar; Vilankurichi Road; Coimbatore; Tamil Nadu 641035; India
Department of Agricultural Biology; Faculty of Agriculture; University of Ruhuna; Mapalana; Kamburupitiya; Sri Lanka
Department of Zoology and Environment Sciences; Faculty of Science; University of Colombo; Colombo; Sri Lanka
Department of Biological Sciences; Faculty of Applied Sciences; Rajarata University of Sri Lanka; Mihintale; Sri Lanka
Sandaraja Wana Arana; Dotel Oya; Aranayaka; Sri Lanka
Department of Agricultural Biology; Faculty of Agriculture; University of Ruhuna; Mapalana; Kamburupitiya; Sri Lanka
Department of Zoology and Environment Sciences; Faculty of Science; University of Colombo; Colombo; Sri Lanka
Centre for Biodiversity and Conservation Studies; Osmania University; Hyderabad; Telangana State 500007; India
Mammalia Molecular phylogeny taxonomy redescription Rhinolophus perniger

Abstract

Insularity provides ample opportunities for species diversification. Sri Lanka is home to a large diversity of species, many of which are endemic but morphologically similar to species found in southern India, due to recent speciation events, suggesting a complex evolutionary history. However, in some taxa although morphological diversity has been noted, the genetic level variations are minimal. Among the wide-ranging horseshoe bats such a phenomenon is noted. In this study, we used bioacoustics, morphometric and molecular data to evaluate the relationships between the taxa of lesser woolly horseshoe bats in the India and Sri Lanka. Our study reveals that the two taxa—Rhinolophus beddomei Andersen, 1905 and here we have validated the existing subspecies from peninsular India and R. sobrinus Andersen, 1918 from Sri Lanka are genetically very close to R. perniger Hodgson, 1843. Currently the taxa—beddomei and sobrinus are recognized as subspecies of Rhinolophus beddomei Andersen, 1905. We provide a detailed description of the taxa beddomei and sobrinus as the original descriptions are limited in nature.

 

References

  1. Agarwal, I., Biswas, S., Bauer, A.M., Greenbaum, E., Jackman, T.R., De Silva, A. & Batuwita, S. (2017) Cryptic species, taxonomic inflation, or a bit of both? New species phenomenon in Sri Lanka as suggested by a phylogeny of dwarf geckos (Reptilia, Squamata, Gekkonidae, Cnemaspis). Systematics and Biodiversity, 15 (5), 427–439. https://doi.org/10.1080/14772000.2017.1282553 DOI: https://doi.org/10.1080/14772000.2017.1282553
  2. Agrawal, V.C. & Sinha, Y.P. (1973) Studies on the bacula of some oriental bats. Anatomischer Anzeiger, 133, 180–192.
  3. Andersen, K. (1905) On the Rhinolophus philippinensis group and five new species. Annals and Magazine of Natural History, 16 (7), 243–257. DOI: https://doi.org/10.1080/03745480509443674
  4. Andersen, K. (1918) Diagnoses of new bats of the families Rhinolophidae and Megadermatidae. Annals and Magazine of Natural History, 2, 374–384. DOI: https://doi.org/10.1080/00222931808562380
  5. Arbogast, B.S. & Slowinski, J.B. (1998) Pleistocene speciation and the mitochondrial DNA clock. Science, 282, 1955a. https://doi.org/10.1126/science.282.5396.1955a DOI: https://doi.org/10.1126/science.282.5396.1955a
  6. Bahir, M.M. & Ng, P.K.L. (2005) Description of ten new species of freshwater crabs (Crustacea: Decapoda: Parathelphusidae: Ceylonthelphusa, Mahatha, Perbrinckia) from Sri Lanka. Raffles Bulletin of Zoology, Supplement, 12, 47–75.
  7. Bates, P.J.J. & Harrison, D.L. (1997) The Bats of the Indian Subcontinent. Harrison Zoological Museum Publications, Sevenoaks, 258 pp.
  8. Batuwita, S. & Bahir, M.M. (2005) Description of five new species of Cyrtodactylus (Reptilia: Gekkonidae) from Sri Lanka. Raffles Bulletin of Zoology, Supplement 12, 351–380.
  9. Bauer, A.M., Jackman, T.R., Greenbaum, E., Giri, V.B. & de Silva, A. (2010) South Asia supports a major endemic radiation of Hemidactylus geckos. Molecular Phylogenetics and Evolution, 57, 342–352. https://doi.org/10.1016/j.ympev.2010.06.014 DOI: https://doi.org/10.1016/j.ympev.2010.06.014
  10. Beenaerts, N., Pethiyagoda, R., Ng, P.K.L., Yeo, D.C.J., Bex, G.J., Bahir, M. & Artois, T. (2010) Phylogenetic diversity of Sri Lankan freshwater crabs and its implications for conservation. Molecular Ecology, 19, 183–196. https://doi.org/10.1111/j.1365-294X.2009.04439.x DOI: https://doi.org/10.1111/j.1365-294X.2009.04439.x
  11. Benda, P. & Vallo, P. (2012) New look on the geographical variation in Rhinolophus clivosus with description of a new horseshoe bat species from Cyrenaica, Libya. Vespertilio, 16, 69–96.
  12. Bogdanowicz, W. & Owen, R.D. (1992) Phylogenetic analysis of the bat family Rhinolophidae. Zeitschrift fur Zoologische Systematik und Evolutionsforschung, 30, 333–338. DOI: https://doi.org/10.1111/j.1439-0469.1992.tb00164.x
  13. Bossuyt, F., Meegaskumbara, M., Beenaerts, N., Gower, D.J., Pethiyagoda, R., Roelants, K., Mannert, A., Wilkinson, M., Bahir, M.M., Manamendra-Arachchi, K., Ng, P.K.L., Schneider, C.J., Oommen, O.V. & Milinkovitch, M.C. (2004) Local endemism within the Western Ghats-Sri Lanka biodiversity hotspot. Science, 306 (5695), 479–481. https://doi.org/10.1126/science.1100167 DOI: https://doi.org/10.1126/science.1100167
  14. Bouckaert, R., Heled, J., Kühnert, D., Vaughan, T., Wu, C.-H., Xie, D., Suchard, M.A., Rambaut, A. & Drummond, A.J. (2014) BEAST 2: A Software Platform for Bayesian Evolutionary Analysis. PLoS Computational Biology, 10 (4), e1003537. https://doi.org/10.1371/journal.pcbi.1003537 DOI: https://doi.org/10.1371/journal.pcbi.1003537
  15. Burgin, C.J., Colella, J.P., Kahn, P.L. & Upham, N.S. (2018) How many species of mammals are there? Journal of Mammalogy, 99, 1–14. https://doi.org/10.1093/jmammal/gyx147 DOI: https://doi.org/10.1093/jmammal/gyx147
  16. Corbet, G.B. & Hill, J.E. (1992) The Mammals of the Indomalayan Region. Natural History Museum and Oxford University Press, Oxford, 488 pp.
  17. Csorba, G., Ujhelyi, P. and Thomas, N. (2003) Horseshoe Bats of the World. Alana Books. Bishop’s Castle, 160 pp.
  18. 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 DOI: https://doi.org/10.1038/nmeth.2109
  19. Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32 (5), 1792–1797. https://doi.org/10.1093/nar/gkh340 DOI: https://doi.org/10.1093/nar/gkh340
  20. Edirisinghe, W.G.M., de Silva, I.M.C., Kusuminda, T.G.T., Thilina, M.H.D.K. & Gunawardana, K.D.S.D. (2016) New breeding data on Rhinolophus beddomei in Sri Lanka: First record of juveniles. Barbastella, 9 (1), 1–4. https://doi.org/10.14709/BarbJ.9.1.2016.03 DOI: https://doi.org/10.14709/BarbJ.9.1.2016.03
  21. Ellerman, J.R. & Morrison-Scott, T.C.S. (1951) Checklist of Palaearctic and Indian mammals 1758 to 1946. British Museum (Natural History), London, 810 pp.
  22. Gower, D.J., Vidal, N., Spinks, J.N. & McCarthy, C.J. (2005) The phylogenetic position of Anomochilidae (Reptilia: Serpentes): First evidence from DNA sequences. Journal of Zoological Systematics and Evolutionary Research, 43, 315–320. https://doi.org/10.1111/j.1439-0469.2005.00315.x DOI: https://doi.org/10.1111/j.1439-0469.2005.00315.x
  23. Grismer, J.L., Schulte, J.A., Alexander, A., Wagner, P., Travers, S.L., Buehler, M.D., Welton, L.J. & Brown, R.M. (2016) The Eurasian invasion: Phylogenomic data reveal multiple Southeast Asian origins for Indian dragon lizards. BioMed Central Evolutionary Biology, 16, 43. https://doi.org/10.1186/s12862-016-0611-6 DOI: https://doi.org/10.1186/s12862-016-0611-6
  24. Gunawardene, N.R., Daniels, A.E.D., Gunatilleke, I.A.U.N., Gunatilleke, C.V.S., Karunakaran, P.V., Geetha Nayak, K., Prasad, S., Puyravaud, P., Ramesh, B.R., Subramanian, K.A. & Vasanthy, G. (2007) A brief overview of the Western Ghats–Sri Lanka biodiversity hotspot. Current Science, 93 (11), 1567–1572.
  25. Hall, T.A. (1999) BioEdit: A User-Friendly Biological Sequence Alignment Editor and Analysis Program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.
  26. Harikrishnan, S., Vasudevan, K., de Silva, A., Deepak, V., Kar, N.B., Naniwadekar, R., Lalremruata, A., Prasoona, K.R. & Aggarwal, R.K. (2012) Phylogeography of Dasia Gray, 1830 (Reptilia: Scincidae), with the description of a new species from southern India. Zootaxa, 3233 (1), 37–51. https://doi.org/10.11646/zootaxa.3233.1.3
  27. Hasegawa, M., Kishino, H. & Yano, T. (1985) Dating of human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution, 22 (2), 160–174. https://doi.org/10.1007/BF02101694 DOI: https://doi.org/10.1007/BF02101694
  28. Hutson, A.M., Rossiter, S.J. & Csorba, G. (2019) Family Rhinolophidae. In: Wilson, D.E. & Mittermeier, R.A. (Eds.), Handbook of the Mammals of the World. Vol. 9. Bats. Lynx Edicions, Barcelona, pp. 260–332.
  29. Hodgson, B.H. (1843) Notice of two marmots inhabiting respectively the plains of Tibet and the Himalayan slopes near to the snows, and also a Rhinolophus of the central region of Nepal. Journal of the Asiatic Society Bengal, 12, 409–414.
  30. Ivanova, N.V., Dewaard, J.R. & Hebert, P.D.N. (2006) An inexpensive, automation-friendly protocol for recovering high-quality DNA. Molecular Ecology Notes, 6, 998–1002. https://doi.org/10.1111/j.1471-8286.2006.01428.x DOI: https://doi.org/10.1111/j.1471-8286.2006.01428.x
  31. 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 DOI: https://doi.org/10.1093/molbev/msy096
  32. Kusuminda, T., Mannakkara, A., Patterson, B.D. & Yapa, W. B. (2018) Bats in tea plantations in Sri Lanka: species richness and distribution. Journal of Bat Research & Conservation, 11 (1), 96–105. DOI: https://doi.org/10.14709/BarbJ.11.1.2018.12
  33. Manamendra-Arachchi, K., Batuwita, S. & Pethiyagoda, R. (2007) A taxonomic revision of the Sri Lankan day-geckos (Reptilia: Gekkonidae: Cnemaspis), with description of new species from Sri Lanka and southern India. Zeylanica, 7, 9–122.
  34. Mao, X.G., Zhu, G.J., Zhang, S. & Rossiter, S.J. (2010) Pleistocene climatic cycling drives intra-specific diversification in the intermediate horseshoe bat (Rhinolophus affinis) in southern China. Molecular Ecology, 19: 2754–2769. https://doi.org/10.1111/j.1365-294X.2010.04704.x DOI: https://doi.org/10.1111/j.1365-294X.2010.04704.x
  35. Mittermier, R.A., Gil, P.R., Hoffmann, M., Pilgrim, J., Brooks, T., Mittermeier, C., Lamoreaux, J., Da Fonseca, G.A.B. & Seligmann, P.A. (2004) Hotspots revisited. Earth’s Biologically Richest and Most Endangered Terrestrial Ecoregions. CEMEX, Mexico, 390 pp.
  36. Myers, N., R.A. Mittermeier, Mittermeier, C.G., da Fonseca, G.A. & Kent, J. (2000) Biodiversity hotspots for conservation priorities. Nature, 403 (6772), 853–858. https://doi.org/10.1038/35002501 DOI: https://doi.org/10.1038/35002501
  37. Patrick, L.E., McCulloch, E.S. & Ruedas, L.A. (2013) Systematics and biogeography of the arcuate horseshoe bat species complex (Chiroptera, Rhinolophidae). Zoologica Scripta, 42 (6), 553–590. https://doi.org/10.1111/zsc.12026 DOI: https://doi.org/10.1111/zsc.12026
  38. Peterhans, J.C.K., Fahr, J., Huhndorf, M.H., Kaleme, P., Plumptre, A.J., Marks, B.D. & Kizungu, R. (2013) Bats (Chiroptera) from the Albertine Rift, eastern Democratic Republic of Congo, with the description of two new species of the Rhinolophus maclaudi group. Bonn Zoological Bulletin, 62 (2), 186–202.
  39. Pfenninger, M. & Schwenk, K. (2007) Cryptic animal species are homogeneously distributed among taxa and biogeographical regions. BMC Evolutionary Biology, 7, 121. https://doi.org/10.1186/1471-2148-7-121 DOI: https://doi.org/10.1186/1471-2148-7-121
  40. Phillips, W.W.A. (1980) Manual of the mammals of Sri Lanka. Part 1. 2nd Revised Edition. Wildlife and Nature Protection Society of Sri Lanka, Colombo, 116 pp.
  41. Pyron, R.A., Kandambi, H.K.D., Hendry, C.R., Pushpamal, V., Burbrink, F.T. & Somaweera, R. (2013) Genus-level molecular phylogeny of snakes reveals the origins of species richness in Sri Lanka. Molecular Phylogenetics and Evolution, 66, 969–975. https://doi.org/10.1016/j.ympev.2012.12.004 DOI: https://doi.org/10.1016/j.ympev.2012.12.004
  42. R Core Team (2018) R: A language and environment for statistical computing. R Foundation for statistical Computing, Vienna. Available from: https://www.R-project.org/ (accessed 15 May 2023)
  43. Rambaut A. (2009) FigTree. Version 1.3.1. Computer program. Available from: http://tree.bio.ed.ac.uk (accessed 15 May 2023)
  44. Rambaut, A., Suchard, M.A. & Drummond, A.J. (2013) Tracer. Version 1.6. Available from: http://tree.bio.ed.ac.uk/software/tracer/ (accessed 15 May 2023)
  45. Simmons, N.B. (2005) Order Chiroptera. In: Wilson, D.E. & Reeder, D.M. (Eds.), Mammal species of the World: a taxonomic and geographic reference. The Johns Hopkins University Press, Baltimore, Maryland, pp. 312–529.
  46. Sinha, Y.P. (1973) Taxonomic studies on the Indian horseshoe bats of the genus Rhinolophus Lacepede. Mammalia, 37 (4), 603–630. DOI: https://doi.org/10.1515/mamm.1973.37.4.603
  47. Soisook, P., Bumrungsri, S., Satasook, C., Thong, V., Bu, S., Harrison, D.L. & Bates, P.J.J. (2008) A taxonomic review of Rhinolophus stheno and R. malayanus (Chiroptera: Rhinolophidae) from continental Southeast Asia: an evaluation of echolocation call frequency in discriminating between cryptic species. Acta Chiropterologica, 10 (2), 221–242. https://doi.org/10.3161/150811008X414818 DOI: https://doi.org/10.3161/150811008X414818
  48. Soisook, P., Karapan, S., Srikrachang, M., Dejtaradol, A., Nualcharoen, K., Bumrungsri, Oo, S.S.L., Aung, M.M., Bates, P.J.J., Harutyunyan, M., Buś, M.M. & Bogdanowicz, W. (2016) Hill forest dweller: a new cryptic species of Rhinolophus in the ‘pusillus group’ (Chiroptera: Rhinolophidae) from Thailand and Lao PDR. Acta Chiropterologica, 18 (1), 117–139. https://doi.org/10.3161/150811009ACC2016.18.1.005 DOI: https://doi.org/10.3161/15081109ACC2016.18.1.005
  49. Soisook, P., Struebig, M.J., Noerfahmy, S., Bernard, H., Maryanto, I., Chen, S., Rossiter, S.J., Kuo, H., Deshpande, K., Bates, P.J.J., Sykes, D. & Miguez, R.P. (2015) Description of a new species of the Rhinolophus trifoliatus-group (Chiroptera: Rhinolophidae) from Southeast Asia. Acta Chiropterologica, 17 (1), 21–36. https://doi.org/10.3161/15081109ACC2015.17.1.002 DOI: https://doi.org/10.3161/15081109ACC2015.17.1.002
  50. Srinivasulu, C. & Srinivasulu, B. (2012) South Asian Mammals: Their diversity, distribution and status. Springer, New York, New York, xii + 467 pp. https://doi.org/10.1007/978-1-4614-3449-8 DOI: https://doi.org/10.1007/978-1-4614-3449-8_2
  51. Srinivasulu, C., Racey, P.A. & Mistry, S. (2010) A key to the bats (Mammalia: Chiroptera) of South Asia. Journal of Threatened Taxa, 2 (7), 1001–1076. https://doi.org/10.11609/JoTT.o2352.1001-76 DOI: https://doi.org/10.11609/JoTT.o2352.1001-76
  52. Srinivasulu, C., Srinivasulu, B., Kaur, H., Shah, T.A. & Devender, G. (2015) New records of Rhinolophus beddomei Andersen, 1905 (Chiroptera: Rhinolophidae) from central peninsular region of India, including echolocation call characteristics. Mammali, 79 (3), 369–373. https://doi.org/10.1515/mammalia-2013-0180 DOI: https://doi.org/10.1515/mammalia-2013-0180
  53. Tate, G.H.H. & Archbold, R. (1939) Results of the Archbold Expeditions. No. 24. Indo-Malayan Rhinolophus, with special reference to material from the Archbold collections. American Museum Novitates, 1036, 12.
  54. Tate, G.H.H. (1943) Further notes on the Rhinolophus philippinensis group (Chiroptera). American Museum Novitates, 1219, 1–5.
  55. Taylor, P.J., Stoffberg, S., Monajdem, A., Schoeman, M.C., Bayliss, J. & Coterill, F.P.D. (2012) Four new bat species (Rhinolophus hilderbrandtii complex) reflect Plio-Pleistocene divergence of dwarfs and giants across an Afromontane Archipelago. PLoS One, 7 (9), 1–23. https://doi.org/10.1371/journal.pone.0041744 DOI: https://doi.org/10.1371/journal.pone.0041744
  56. Topál, G. (1958) Morphological studies on the os penis of bats in the Carpathian Basin. Annales historico-naturales Musei nationalis hungarici, 50, 331–342, 2 figs, 2 pls.
  57. Topál, G. & Csorba, G. (1992) The subspecific division of Rhinolophus luctus Temminck, 1835, and the taxonomic status of R. beddomei Andersen, 1905 (Mammalia: Chiroptera). Miscellanea Zoologica Hungarica, 7, 101–116.
  58. Thapa, S. (2018) Habitat and acoustic survey and an action plan for bats conservation in the Kathmandu Valley, Nepal. Final report submitted to Rufford Small Grants. Available from: https://www.rufford.org/projects/sanjan-thapa (accessed 15 May 2023)
  59. Vaz, G.G. (2000) Age of relict coral reef from the continental shelf off Karaikal, Bay of Bengal: Evidence of last glacial maximum. Current Science, 79 (2), 228–230.
  60. Volleth, M., Loidl, J., Mayer, F., Yong, H.-S., Müller, S. & Heller, K.-G. (2015) Surprising Genetic Diversity in Rhinolophus luctus (Chiroptera: Rhinolophidae) from Peninsular Malaysia: Description of a New Species Based on Genetic and Morphological Characters. Acta Chiropterologica, 17 (1), 1–20. https://doi.org/10.3161/15081109acc2015.17.1.001 DOI: https://doi.org/10.3161/15081109ACC2015.17.1.001
  61. Volleth, M., Anwarali Khan, F., Müller, S, & Arenas, D, Baker, R., Stevens, R., Trifonov, V., Liehr, T., Heller, K.-G. & Sotero-Caio, C. (2021) Cytogenetic investigations in Bornean Rhinolophoidea revealed cryptic diversity in Rhinolophus sedulus entailing classification of peninsular Malaysia specimens as a new species. Acta Chiropterologica, 23 (1), 1–20. https://doi.org/10.3161/15081109ACC2021.23.1.001 DOI: https://doi.org/10.3161/15081109ACC2021.23.1.001
  62. Wu, W., Ng, W.-L., Yang, J.-X., Li ,W.-M. & Ge, X.-J. (2018) High cryptic diversity is revealed by genome-wide polymorphisms in a wild relative of banana, Musa iterans, and implications for its conservation in subtropical China. BMC Plant Biology, 18, 194. https://doi.org/10.1186/s12870-018-1410-6 DOI: https://doi.org/10.1186/s12870-018-1410-6
  63. Wu, Y., Harada, M. & Motokawa, M. (2009) Taxonomy of Rhinolophus yunanensis Dobson, 1872 (Chiroptera: Rhinolophidae) with a description of a new species from Thailand. Acta Chiropterologica, 11 (2), 237–246. https://doi.org/10.3161/150811009X485486 DOI: https://doi.org/10.3161/150811009X485486
  64. Wu, Y., Motokawa, M. & Harada, M. (2008) A New species of Horseshoe bat of the Genus Rhinolophus from China (Chiroptera: Rhinolophidae). Zoological Science, 25(4): 438–443. https://doi.org/10.2108/zsj.25.438 DOI: https://doi.org/10.2108/zsj.25.438
  65. Wu, Y. & Thong, V.D. (2011) A new species of Rhinolophus (Chiroptera: Rhinolophidae) from China. Zoological Science, 28, 235–241. https://doi.org/10.2108/zsj.28.235 DOI: https://doi.org/10.2108/zsj.28.235