Integrated approaches to identifying cryptic bat species in areas of high endemism: The case of Rhinolophus andamanensis in the Andaman Islands

Autoři: Chelmala Srinivasulu aff001;  Aditya Srinivasulu aff003;  Bhargavi Srinivasulu aff001;  Gareth Jones aff004
Působiště autorů: Natural History Museum and Wildlife Biology & Taxonomy Lab, Department of Zoology, University College of Science, Osmania University, Hyderabad, Telangana, India aff001;  Systematics, Ecology & Conservation Laboratory, Zoo Outreach Organisation (ZOO), Saravanampatti, Coimbatore, Tamil Nadu, India aff002;  Biodiversity Research and Conservation Society, Tirumalgiri, Secunderabad, Telangana, India aff003;  School of Biological Sciences, Bristol, United Kingdom aff004
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article


The diversity of bats worldwide includes large numbers of cryptic species, partly because divergence in acoustic traits such as echolocation calls are under stronger selection than differences in visual appearance in these nocturnal mammals. Island faunas often contain disproportionate numbers of endemic species, and hence we might expect cryptic, endemic species to be discovered relatively frequently in bats inhabiting islands. Species are best defined when multiple lines of evidence supports their diagnosis. Here we use morphometric, acoustic, and molecular phylogenetic data to show that a horseshoe bat in the Andaman Islands is distinct in all three aspects, supporting its status as a distinct species. We recommend investigation into possible new and endemic bat species on islands by using integrated approaches that provide independent lines of evidence for taxonomic distinctiveness. We provide a formal redescription of the taxon newly raised to species level, Rhinolophus andamanensis Dobson, 1872.

Klíčová slova:

Bats – Ears – Echolocation – Islands – Morphometry – Phylogenetic analysis – Cryptic speciation


1. Bickford D, Lohman DJ, Sodhi NS, Ng PK, Meier R, Winker K, et al. Cryptic species as a window on diversity and conservation. Trends Ecol. Evol. 2007; 22:148–55. doi: 10.1016/j.tree.2006.11.004 17129636

2. Burgin CJ, Colella JP, Kahn PL Upham NS. How many species of mammals are there? Jour. Mamm. 2018; 99: 1–14.

3. Wilson DE, Reeder DM, editors. Mammal species of the world: a taxonomic and geographic reference. 1st ed. Washington, D.C.: Smithsonian Institution Press; 1993.

4. Jones G, Barlow KE. Cryptic species of echolocating bats. In: Thomas JA, Moss CF, Vater M, editors. Echolocation in bats and dolphins. Chicago, IL: University of Chicago Press; 2004. p. 345–349.

5. Jones G, van Parijs SM. Bimodal echolocation in pipistrelle bats: Are cryptic species present? Proc. Roy. Soc. Lond. 1993; B251:119–25.

6. Mayer F, Dietz C, Kiefer A. Molecular species identification boosts bat diversity. Front. Zool. 2007; 4(4): 1–5.

7. Clare EL. Cryptic species? Patterns of maternal and paternal gene flow in eight neotropical bats. PLoS ONE 2011; species.

8. Singhal S, Hoskin CJ, Couper P, Potter S, Moritz C. A framework for resolving cryptic species: A case study from the lizards of the Australian wet tropics. Syst. Bio. 2018;

9. Herdina AN, Hulva P, Horáček I, Benda P, Mayer C, Hilgers, et al. MicroCT imaging reveals morphometric baculum differences for discriminating the cryptic species Pipistrellus pipistrellus and P. pygmaeus. Acta Chiropterol. 2014; 16(1):157–68.

10. Jones G. Acoustic signals and speciation: The roles of natural and sexual selection in the evolution of cryptic species. Adv. Study Behav. 1997; 26:317–54.

11. Barratt EM, Deaville R, Burland TM, Bruford MW, Jones G, Racey PA et al. DNA answers the call of pipistrelle bat species. Nature 1997; 387:138–139.

12. Francis CM, Borisenko AV, Ivanova NV, Eger JL, Lim BK, Guillén-Servent A, et al. The role of DNA barcodes in understanding and conservation of mammal diversity in Southeast Asia. PLoS ONE 2010; 5(9): e12575. doi: 10.1371/journal.pone.0012575 20838635

13. Pande P, Kothari A, Singh S, editors. Directory of national parks and sanctuaries in Andaman and Nicobar Islands: Management status and profiles. New Delhi: IIPA; 1991.

14. Myers N, Mittermeier RA, Mittermeier CG, daFonseca GAB, Kent J. Biodiversity hotspots for conservation priorities. Nature 2000; 403: 853–58. doi: 10.1038/35002501 10706275

15. Bandopadhyay PC, Carter A. Geological framework of the Andaman—Nicobar Islands. GSL Mem. 2017: 47: 75–93.

16. Curray JR. Tectonics and history of the Andaman Sea region. J. Asian Earth Sci. 2005; 25: 187–232.

17. Raju KAK, Ramprasad T, Rao PS, Rao BR, Varghese J. New insights into the tectonic evolution of the Andaman basin, northeast Indian Ocean. Earth Planet. Sci. Lett. 2004; 221: 145–62.

18. Dobson GE. Brief description of five new species of rhinolophine bats. J. Asiat. Soc. Beng. 1872; 41: 336–38.

19. Ellerman JR, Morrison-Scott RCS. Checklist of Palearctic and Indian Mammals. London: British Museum of Natural History; 1951.

20. Sinha YP. Taxonomic studies on the Indian horseshoe bats of the genus Rhinolophus Lacepede. Mammalia 1973; 37(4): 603–30.

21. Corbet GB, Hill JE. The Mammals of the Indo-Malayan Region. Oxford: Natural History Museum Publications & Oxford University Press; 1992.

22. Bates PJJ, Harrison DL. Bats of the Indian Subcontinent. Sevenoaks: Harrison Zoological Museum; 1997.

23. Simmons NB. Order Chiroptera. In: Wilson DE, Reeder DM, editors. Mammal Species of the World: A taxonomic and geographic reference. 3rd ed., Vol. 1. Baltimore: Johns Hopkins University Press; 2005.

24. Srinivasulu C, Srinivasulu B. South Asian Mammals: Their diversity, distribution and status. New York: Springer; 2012.

25. Ghosh MK. Catalogue of Chiroptera in the collection of Zoological Survey of India (Part-II: Microchiroptera). Rec. Zool. surv. lndia, Occc. Pap. 2008; 281: 1–339.

26. Aul B, Bates PJJ, Harrison DL, Marimuthu G. Diversity, distribution and status of bats on the Andaman and Nicobar Islands, India. Oryx, 2014; 48: 204–12.

27. Srinivasulu C, Srinivasulu A, Srinivasulu B, Gopi A, Tauseef HD, Bates PJJ, et al. Recent surveys of bats from the Andaman Islands, India: Diversity, distribution, and echolocation characteristics. Acta Chiropterol. 2017; 19(2): 419–37.

28. Sikes RS. 2016 Guidelines of the American Society of Mammalogists for the use of wild mammals in research and education. J. Mammal. 2016; 97(3): 663–88. doi: 10.1093/jmammal/gyw078 29692469

29. Gy Topal. Morphological studies on the os penis of bats in the Carpathian Basin. Ann. Hist-nat. Mus. Natl. Hung., 1958; ser. nov. 9: 331–42.

30. Ith S, Bumrungsri S, Thomas NM, Bates PJJ, Willette DA, Khan FAA, et al. Geographical variation of Rhinolophus affinis (Chiroptera: Rhinolophidae) in the Sundaic subregion of Southeast Asia, including the Malay Peninsula, Borneo and Sumatra. Acta Chiropterol. 2016; 18(1): 141–61.

31. Kuhn M. caret: Classification and Regression Training. R package version 6.0–84. 2019.

32. R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2013.

33. Ivanova NV, Dewaard JR, Hebert PDN. An inexpensive, automation-friendly protocol for recovering high-quality DNA. Mol. Ecol. Notes 2006; 6: 998–1002.

34. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004; 32(5): 1792–97. doi: 10.1093/nar/gkh340 15034147

35. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Mol. Biol. Evol. 2013; 30(12): 2725–29. doi: 10.1093/molbev/mst197 24132122

36. Guindon S, Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol., 2003; 52(5): 696–704. doi: 10.1080/10635150390235520 14530136

37. Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods 2012; 9(8): 772.

38. Hasegawa M, Iida Y, Yano T, Takaiwa F, Iwabuchi M. Phylogenetic relationships among eukaryotic kingdoms inferred from ribosomal RNA sequences. J. Mol. Evol. 1985; 22(1): 32–8. doi: 10.1007/bf02105802 3932662

39. Mao XG, Zhu GJ, Zhang S, Rossiter SJ. Pleistocene climatic cycling drives intra-specific diversification in the intermediate horseshoe bat (Rhinolophus affinis) in southern China. Mol. Ecol. 2010; 19: 2754–69. doi: 10.1111/j.1365-294X.2010.04704.x 20561192

40. Drummond AJ, Suchard MA, Xie D, Rambaut A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 2012; 29(8): 1969–73. doi: 10.1093/molbev/mss075 22367748

41. Rambaut A, Suchard MA, Drummond AJ. Tracer v1.6 [software]. 2013. URL

42. Rambaut A. FigTree version 1.3.1 [software]. 2009. URL

43. Bates PJ, Thi MM, Nwe TH, Bu SS, Mie KM, Nyo N, Khaing AA, Aye NN, Oo T, Mackie IC. A review of Rhinolophus (Chiroptera: Rhinolophidae) from Myanmar, including three species new to the country. Acta Chiropterol. 2004; 6(1): 23–48.

44. Yi Wu, Harada M, Motokawa M. Taxonomy of Rhinolophus yunanensis (Chiroptera: Rhinolophidae) with a description of a new species from Thailand. Acta Chiropterol. 2009; 11(2): 237–246.

45. Ith S, Bumrungsri S, Thomas NM, Bates PJJ, Wonglapsuwan M, Khan FAA, et al. Taxonomical implications of geographical variation in Rhinolophus affinis (Chiroptera: Rhinolophidae) in mainland Southeast Asia. Zool. Stud. 2015; 54: 31.

46. Jones G. Scaling of echolocation call parameters in bats. J Exp. Biol., 1999; 202: 3359–67. 10562518

47. Chakravarty R, Chattopadhyay B, Ramakrishnan U, Sivasundar A. Comparative population structure in species of bats differing in ecology and morphology in the Andaman Islands, India. Acta Chiropterol. 2018: 20(1): 85–98.

48. MacArthur RH, Wilson EO. The theory of island biogeography. Princeton: Princeton University Press; 1967.

49. Price TD, Phillimore AB, Awodey M, Hudson R. Ecological and geographical influences on the allopatric phase of island speciation. In: Grant PR, Grant BR, editors. In search of the causes of evolution: From field observations to mechanisms. Princeton: Princeton University Press; 2010. p. 251–81.

50. Rosindell J, Phillimore AB. A unified model of island biogeography sheds light on the zone of radiation. Ecol. Lett. 2011; 14: 552–60. doi: 10.1111/j.1461-0248.2011.01617.x 21481125

51. Fleming TH, Racey PA. Island bats: evolution, ecology and conservation. Chicago: Chicago University Press; 2009.

52. Conenna I, Rocha R, Russo D, Cabeza M. Insular bats and research effort: a review of global patterns and priorities. Mamm. Rev. 2017; 47: 169–82.

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