Abstract
The genus Miniopterus is highly diverse in cryptic species. Based on integrated approaches of morphometrics, echolocation call analysis, and molecular phylogenetics, we present evidence of a hitherto undescribed species, Srini’s Bent-winged bat Miniopterus srinii sp. nov.. The new species, found in the Western Ghats of southern Karnataka, India, closely resembles the Small Bent-winged bat Miniopterus pusillus, found elsewhere in Karnataka, Kerala, and Tamil Nadu, India. Although it shows external similarity with Miniopterus pusillus sensu stricto from the Nicobar Islands, the new species is relatively larger and distinct in craniodental measurements and echolocation call parameters, despite slight overlaps. Importantly, Miniopterus srinii exhibits morphological convergence with Miniopterus pusillus as despite similarities in morphologies, there is a significant genetic distance of 10.84 ± 0.22%. The new cryptic species shares distribution with Miniopterus phillipsi and Miniopterus pusillus in the Western Ghats, further highlighting the need to study both the genus’ cryptic diversity, and the region’s conservation importance.
References
- Agnarsson, I., Zambrana-Torrelio, C.M., Flores-Saldana, N.P. & May-Collado, L.J. (2011) A time-calibrated species-level phylogeny of bats (Chiroptera, Mammalia). PLoS Currents, 3, RRN1212. https://doi.org/10.1371/currents.RRN1212 DOI: https://doi.org/10.1371/currents.RRN1212
- Arbogast, B.S., Edwards, S.V., Wakeley, J., Beerli, P. & Slowinski, J.B. (2002) Estimating divergence times from Molecular data on phylogenetic and population genetic timescales. Annual Review of Ecology Evolution and Systematics, 33, 707–740. https://doi.org/10.1146/annurev.ecolsys.33.010802.150500 DOI: https://doi.org/10.1146/annurev.ecolsys.33.010802.150500
- Armstrong, K.N., Wiantoro, S. & Aplin, K. (2021) Miniopterus magnater (amended version of 2019 assessment). The IUCN Red List of Threatened Species, 2021, e.T13566A209529644. https://doi.org/10.2305/IUCN.UK.2021-3.RLTS.T13566A209529644.en DOI: https://doi.org/10.2305/IUCN.UK.2021-3.RLTS.T13566A209529644.en
- Bates, P.J.J. & Harrison, D.L. (1997) The Bats of the Indian Subcontinent. Harrison Zoological Museum Publications, Sevenoaks, 258 pp.
- Bickford, D., Lohman, D.J., Sodhi, N.S., Ng, P.K.L., Meier, R., Winker, K., Ingram, K.K. & Das, I. (2007) Cryptic species as a window on diversity and conservation. Trends in Ecology and Evolution, 22 (3), 148–155. https://doi.org/10.1016/j.tree.2006.11.004 DOI: https://doi.org/10.1016/j.tree.2006.11.004
- Bonaparte, C.L. (1837) Iconografia della fauna italica: Per le quattro classi degli animali vertebrati. Tipografia Salviucci, Rome, 1104 pp.
- Brook, B.W., Bradshaw, C.J.A., Koh, L.P. & Sodhi, N.S. (2006) Momentum Drives the Crash: Mass Extinction in the Tropics. Biotropica, 38, 302–305. https://doi.org/10.1111/j.1744-7429.2006.00141.x DOI: https://doi.org/10.1111/j.1744-7429.2006.00141.x
- Bruford, M.W., Hanotte, O., Brookfield, J.F.Y. & Burke, T. (1992) Single locus and multilocus DNA fingerprinting. In: Hoelzel, R. (Ed.), Molecular Genetic Analysis of Populations: a Practical Approach. IRL Press, Oxford, pp. 225–269.
- Bumrungsri, S., Bates, P.J.J., Molur, S., Srinivasulu, C. & Furey, N. (2021) Miniopterus pusillus. The IUCN Red List of Threatened Species, 2021, e.T13569A22103542. https://doi.org/10.2305/IUCN.UK.2021-2.RLTS.T13569A22103542.en DOI: https://doi.org/10.2305/IUCN.UK.2021-2.RLTS.T13569A22103542.en
- CEPF (2016) Final Assessment of CEPF Investment in the Western Ghats Region of the Western Ghats and Sri Lanka Biodiversity Hotspot. Ashoka Trust for Research in Ecology and the Environment, Critical Ecosystem Partnership Fund, 73 pp. [https://www.cepf.net/sites/default/files/western-ghats-final-assessment-2016-english.pdf]
- Chakravarty, R., Ruedi, M. & Ishtiaq, F. (2020) A recent survey of bats with descriptions of echolocation calls and new records from the western Himalayan region of Uttarakhand, India. Acta Chiropterologica, 22 (1), 197–224. https://doi.org/10.3161/15081109ACC2020.22.1.019 DOI: https://doi.org/10.3161/15081109ACC2020.22.1.019
- Christidis, L., Goodman, S.M., Naughton, K. & Appleton, B. (2014) Insights into the evolution of a cryptic radiation of bats: dispersal and ecological radiation of Malagasy Miniopterus (Chiroptera: Miniopteridae). PLoS ONE, 9, e92440. https://doi.org/10.1371/journal.pone.0092440 DOI: https://doi.org/10.1371/journal.pone.0092440
- 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
- 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
- Edler, D., Klein, J., Antonelli, A. & Silvestro, D. (2020) raxmlGUI 2.0: A graphical interface and toolkit for phylogenetic analyses using RAxML. Methods in Ecology and Evolution, 12, 373–377. https://doi.org/10.1111/2041-210X.13512 DOI: https://doi.org/10.1111/2041-210X.13512
- 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.
- Esselstyn, J.A., Widmann, P. & Heaney, L.R. (2004) The mammals of Palawan Island, Philippines. Proceedings of the Biological Society of Washington, 117 (3), 271–302.
- Ghosh, M.K. (2008) Catalogue of Chiroptera in the collection of Zoological Survey of India (Part-II: Microchiroptera). Records of the Zoological Survey of India, Occasional Paper, No. 281, 1–339.
- Goodman, S.M., Maminirina, C.P., Weyeneth, N., Bradman, H.M., Christidis, L.L., Ruedi, M. & Appleton, B. (2009) The use of molecular and morphological characters to resolve the taxonomic identity of cryptic species: the case of Miniopterus manavi (Chiroptera, Miniopteridae). Zoologica Scripta, 38 (4), 339–363. https://doi.org/10.1111/j.1463-6409.2008.00377.x DOI: https://doi.org/10.1111/j.1463-6409.2008.00377.x
- Goodman, S.M., Ramasindrazana, B., Maminirina, C.P., Schoeman, M.C. & Appleton, B. (2011) Morphological, bioacoustical, and genetic variation in Miniopterus bats from eastern Madagascar, with the description of a new species. Zootaxa, 2880 (1), 1–19. https://doi.org/10.11646/zootaxa.2880.1.1 DOI: https://doi.org/10.11646/zootaxa.2880.1.1
- Goodman, S.M., Ramasindrazana, B., Naughton, K.M. & Appleton, B. (2015) Description of a new species of the Miniopterus aelleni group (Chiroptera: Miniopteridae) from upland areas of central and northern Madagascar. Zootaxa, 3936 (4), 538–558. https://doi.org/10.11646/zootaxa.3936.4.4 DOI: https://doi.org/10.11646/zootaxa.3936.4.4
- Goodman, S.M., Ryan, K.E., Maminirina, C.P., Fahr, J., Christidis, L.L. & Appleton, B.R. (2007) Specific status of populations on Madagascar referred to Miniopterus fraterculus (Chiroptera: Vespertilionidae), with description of a new species. Journal of Mammalogy, 88, 1216–1229. https://doi.org/10.1644/06-MAMM-A-285R1.1 DOI: https://doi.org/10.1644/06-MAMM-A-285R1.1
- Hayman, R.W. & Hill, J.E. (1971) Part 2: Order Chiroptera. In: Meester, J. & Setzer, H.W. (Eds.), The mammals of Africa. An identification manual. Smithsonian Institution Press, Washington, D.C., pp. 1–73.
- Hill, J.E. (1983) Bats (Mammalia: Chiroptera) from Indo-Australia. Bulletin of the British Museum of Natural History, Zoology Series, 45, 103–208. https://doi.org/10.5962/p.27997 DOI: https://doi.org/10.5962/p.27997
- Hughes, A.C., Satasook, C., Bates, P.J.J., Soisook, P., Sritongchuay, T., Jones, G. & Bumrungsri, S. (2011) Using echolocation calls to identify Thai bat species: Vespertilionidae, Emballonuridae, Nycteridae and Megadermatidae. Acta Chiropterologica, 13 (2), 447–455. https://doi.org/10.3161/150811011X624938 DOI: https://doi.org/10.3161/150811011X624938
- Ibáñez, C. & Juste, J. (2019) Family Miniopteridae (Long-fingered Bats). In: Wilson, D.E. & Mittermeier, R.A. (Eds.), Handbook of the Mammals of the World. Vol. 9. Bats. Lynx Edicions, Barcelona, pp. 674–709.
- 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
- Jones, G. (2009) Bats in China. Available from: http://www.bio.bris.ac.uk/research/bats/China%20bats/ (accessed 21 May 2022)
- Jones, G., Jacobs, D.S., Kunz, T.H., Willing, M.H. & Racey, P.A. (2009) Carpe noctem: the importance of bats as bioindicators. Endangered Species Research, 8, 93–115. https://doi.org/10.3354/esr00182 DOI: https://doi.org/10.3354/esr00182
- Kitchener, D.J. & Suyanto, A. (2002) Morphological variation in Miniopterus pusillus and M. australis (sensu Hill 1992) in southeastern Asia, New Guinea, and Australia. Records of the Western Australian Museum, 21, 9–33. https://doi.org/10.18195/issn.0312-3162.21(1).2002.009-033 DOI: https://doi.org/10.18195/issn.0312-3162.21(1).2002.009-033
- Kruskop, S.V. (2021) Diversity Aspects in Bats: Genetics, Morphology, Community Structure. Diversity, 13, 424. https://doi.org/10.3390/d13090424 DOI: https://doi.org/10.3390/d13090424
- Kumar, S., Stecher, G. & Tamura, K. (2015) MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Molecular Biology and Evolution, 33 (7), 1870–1874. https://doi.org/10.1093/molbev/msw054 DOI: https://doi.org/10.1093/molbev/msw054
- Kusuminda, K., Mannakkara, A., Ukuwela, K.D.B., Kruskop, S.V., Amarasinghe, C.J., Saikia, U., Venugopal, P., Karunarathna, M., Gamage, R., Ruedi, M., Csorba, G., Yapa, W.B. & Patterson, B.D. (2022) DNA barcoding and morphological analyses reveal a cryptic species of Miniopterus from India and Sri Lanka. Acta Chiropterologica, 24 (1), 1–17. https://doi.org/10.3161/15081109ACC2022.24.1.001 DOI: https://doi.org/10.3161/15081109ACC2022.24.1.001
- Kuznetsov, A.N., Su, K., Phan, L., Alex, B., Van, N., Vladimir, B. & Andrei, Z. (2015) s.n. Bat Report—Cat Tien, 2001, 1–45.
- Letunic, I. & Bork, P. (2021) Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Research, 49 (W1), W293–W296. https://doi.org/10.1093/nar/gkab301 DOI: https://doi.org/10.1093/nar/gkab301
- Maeda, K. (1982) Studies on the classification of Miniopterus in Eurasia, Australia and Melanesia. Honyurui Kagaku (Mammalian Science), Supplement 1, 1–176.
- Medlin, L.K. (1997) Can molecular techniques help define species limits? Diatom, 13, 19–23.
- Miller-Butterworth, C.M., Eick, G., Jacobs, D.S., Schoeman, M.C. & Harley, E.H. (2005) Genetic and phenotypic differences between South African long-fingered bats, with a global Miniopterine phylogeny. Journal of Mammalogy, 86 (6), 1121–1135. https://doi.org/10.1644/05-MAMM-A-021R1.1 DOI: https://doi.org/10.1644/05-MAMM-A-021R1.1
- Monadjem, A., Goodman, S.M., Stanley, W.T. & Appleton, B. (2013) A cryptic new species of Miniopterus from south-eastern Africa based on molecular and morphological characters. Zootaxa, 3746 (1), 123–142. https://doi.org/10.11646/zootaxa.3746.1.5 DOI: https://doi.org/10.11646/zootaxa.3746.1.5
- Monadjem, A., Guyton, J., Naskrecki, P., Richards, L.R., Kropff, A.S. & Dalton, D.L. (2020) Cryptic diversity in the genus Miniopterus with the description of a new species from southern Africa. Acta Chiropterologica, 22 (1), 1–19. https://doi.org/10.3161/15081109ACC2020.22.1.001 DOI: https://doi.org/10.3161/15081109ACC2020.22.1.001
- Monadjem, A., Shapiro, J.T., Richards, L.R., Karabulut, H., Crawley, W., Nielsen, I.B., Hansen, A., Bohmann, K. & Mourier, M. (2019) Systematics of West African Miniopterus with the description of a new species. Acta Chiropterologica, 21 (2), 237–256. https://doi.org/10.3161/15081109ACC2019.21.2.001 DOI: https://doi.org/10.3161/15081109ACC2019.21.2.001
- Myers, N., Mittermeier, R.A., Mittermeier, C.G., da Fonseca, G.A.B. & Kent, J. (2000) Biodiversity hotspots for conservation priorities. Nature, 403, 853–858. https://doi.org/10.1038/35002501 DOI: https://doi.org/10.1038/35002501
- Osipova, E., Emslie-Smith, M., Osti, M., Murai, M., Åberg, U. & Shadie, P. (2020) IUCN World Heritage Outlook 3: A conservation assessment of all natural World Heritage sites, November 2020. IUCN, International Union for Conservation of Nature, Gland, 90 pp. https://doi.org/10.2305/IUCN.CH.2020.16.en DOI: https://doi.org/10.2305/IUCN.CH.2020.16.en
- Phauk, S., Phen, S. & Furey, N.M. (2013) Cambodian bat echolocation: a first description of assemblage call parameters and assessment of their utility for species identification. Cambodian Journal of Natural History, 1, 16–26.
- Puechmaille, S.J., Allegrini, B., Benda, P., Gürün, K., Šrámek, J., Ibañez, C., Juste, J. & Bilgin, R. (2014) A new species of the Miniopterus schreibersii species complex (Chiroptera: Miniopteridae) from the Maghreb Region, North Africa. Zootaxa, 3794 (1), 108–124. https://doi.org/10.11646/zootaxa.3794.1.4 DOI: https://doi.org/10.11646/zootaxa.3794.1.4
- Puechmaille, S.J., Ar Gouilh, M., Piyapan, P., Yokubol, M., Mie, K.M., Bates, P.J.J., Satasook, C., Nwe, T., Bu, S.S.H., Mackie, I.J., Petit, E.J. & Teeling, E.C. (2011) The evolution of sensory divergence in the context of limited gene flow in the bumblebee bat. Nature Communications, 2, 573. https://doi.org/10.1038/ncomms1582 DOI: https://doi.org/10.1038/ncomms1582
- Raman, S. & Hughes, A.C. (2020) Echobank for the bats of Western Ghats biodiversity hotspot, India. Acta Chiropterologica, 22 (2), 349–364. https://doi.org/10.3161/15081109ACC2020.22.2.010 DOI: https://doi.org/10.3161/15081109ACC2020.22.2.010
- Raman, S., Padmarajan, A., Faizal, M.A., Das, A.A., Ushakumari, P., Singh, S. & Hughes, A.C. (2021) Annotated checklist, distribution and regional status of the bats (Mammalia: Chiroptera) of Kerala, South India. Journal of Bat Research & Conservation, 14 (1), 183–207. https://doi.org/10.14709/BarbJ.14.1.2021.17 DOI: https://doi.org/10.14709/BarbJ.14.1.2021.17
- Ramasindrazana, B., Goodman, S.M., Schoeman, M.C. & Appleton, B. (2011) Identification of cryptic species of Miniopterus bats (Chiroptera: Miniopteridae) from Madagascar and the Comoros using bioacoustics overlaid on molecular genetic and morphological characters. Biological Journal of the Linnean Society, 104, 284–302. https://doi.org/10.1111/j.1095-8312.2011.01740.x DOI: https://doi.org/10.1111/j.1095-8312.2011.01740.x
- Rambaut, A., Suchard, M.A. & Drummond, A.J. (2013) Tracer. Version 1.6. Software. Available from: http://tree.bio.ed.ac.uk/software/tracer/ (accessed 8 March 2023)
- Saikia, U., Thabah, A. & Ruedi, M. (2020) Taxonomic and ecological notes on some poorly known bats (Mammalia: Chiroptera) from Meghalaya, India. Journal of Threatened Taxa, 12 (3), 15311–15325. https://doi.org/10.11609/jott.5264.12.3.15311-15325 DOI: https://doi.org/10.11609/jott.5264.12.3.15311-15325
- Schönrogge, K., Barr, B., Wardlaw, J.C., Napper, E., Gardner, M.G., Breen, J., Elmes, G.W. & Thomas, J.A. (2002) When rare species become endangered: Cryptic speciation in myrmecophilous hoverflies. Biological Journal of the Linnean Society, 75 (3), 291–300. https://doi.org/10.1111/j.1095-8312.2002.tb02070.x DOI: https://doi.org/10.1111/j.1095-8312.2002.tb02070.x
- Sikes, R.S. (2016) Guidelines of the American Society of Mammalogists for the use of wild mammals in research and education. Journal of Mammalogy, 97 (3), 663–688. https://doi.org/10.1093/jmammal/gyw078 DOI: https://doi.org/10.1093/jmammal/gyw078
- Skinner, J.D. & Smithers, R.H.N. (1990) The Mammals of the southern African subregion. 2nd Edition, University of Pretoria Press, Pretoria, 771 pp.
- Srinivasulu, A., Srinivasulu, B. & Srinivasulu, C. (2021) Ecological niche modelling for the conservation of endemic threatened squamates (lizards and snakes) in the Western Ghats. Global Ecology and Conservation, 28 (2021) e01700. https://doi.org/10.1016/j.gecco.2021.e01700 DOI: https://doi.org/10.1016/j.gecco.2021.e01700
- Srinivasulu, B. & Srinivasulu, C. (2017) A first record of three hitherto unreported species of bats from Kerala, India with a note on Myotis peytoni (Mammalia: Chiroptera: Vespertilionidae). Journal of Threatened Taxa, 9 (5), 10216–10222. https://doi.org/10.11609/jott.3324.9.5.10216-10222 DOI: https://doi.org/10.11609/jott.3324.9.5.10216-10222
- Srinivasulu, C., Srinivasulu, A. & Srinivasulu, B. (2023) Checklist of the bats of India. Version 1.6. Available from: https://threatenedtaxa.org/index.php/JoTT/checklists/bats/india (accessed 6 March 2023)
- Srinivasulu, C., Srinivasulu, A., Srinivasulu, B. & Jones, G. (2019) Integrated approaches to identifying cryptic bat species in areas of high endemism: The case of Rhinolophus andamanensis in the Andaman Islands. PLOS One, 14 (10), e0213562. https://doi.org/10.1371/journal.pone.0213562 DOI: https://doi.org/10.1371/journal.pone.0213562
- 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
- Srinivasulu, C., Srinivasulu, B. & Molur, S. (Compilers) (2014) The Status and Distribution of Reptiles in the Western Ghats, India. Conservation Assessment and Management Plan (CAMP). Wildlife Information Liaison Development Society., Coimbatore, Tamil Nadu, viii+148 pp.
- Suchard, M.A., Lemey, P., Baele, G., Ayres, D.L., Drummond, A.J. & Rambaut, A. (2018) Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evolution, 4, vey016. https://doi.org/10.1093/ve/vey016 DOI: https://doi.org/10.1093/ve/vey016
- Vaughan, T.G. (2017) IcyTree: Rapid browser-based visualization for phylogenetic trees and networks. Bioinformatics, 33 (15), 2392–2394. https://doi.org/10.1093/bioinformatics/btx155 DOI: https://doi.org/10.1093/bioinformatics/btx155
- Wordley, C.F.R., Foui, E.K., Mudappa, D., Sankaran, M. & Altringham, J.D. (2014) Acoustic identification of bats in the southern Western Ghats, India. Acta Chiropterologica, 16, 213–222. https://doi.org/10.3161/150811014X683408 DOI: https://doi.org/10.3161/150811014X683408
- Wroughton, R.C. (1918) Summary of the results from the Indian mammal survey. Parts 1&2. Journal Bombay Natural History Society, 25 & 26, 547–598 & 19–58.
- Wu, H., Jiang, T., Liu, S., Lu, G. & Feng, J. (2019) Acoustic identification of two morphologically similar bat species, Miniopterus magnater and Miniopterus fuliginosus (Chiroptera, Miniopteridae). Mammalia, 84 (2), 201–206. https://doi.org/10.1515/mammalia-2018-0197 DOI: https://doi.org/10.1515/mammalia-2018-0197
- Yoshiyuki, M. (1989) A systematic study of the Japanese Chiroptera. National Science Museum monographs, 7, 1–242.