Abstract
Kondana soft-furred rat is a critically endangered (CR) species, known from a single locality – Sinhgad in the northern Western Ghats, India. However, the taxonomic status of this species is uncertain due to its close resemblance to the widely distributed soft-furred field rat Millardia meltada, which has serious implications on the conservation status of Millardia kondana. In this study, we assessed the current taxonomic status of M. kondana through an integrative approach combining morphological, molecular and environmental niche modeling analyses. We collected morphological data from the specimens around Sinhgad as well as preserved specimens in the museum. Both morphological and two-dimensional (2D) morphometrical analyses showed a significant difference between M. kondana and M. meltada. Molecular phylogeny based on cytochrome b gene revealed a sister relationship between M. kondana and M. meltada, and both species form distinct well-supported monophyletic clades. Niche modeling also predicted niche segregation between the two species: M. kondana preferred areas with a high elevation and precipitation seasonality while M. meltada favored regions with a low elevation and precipitation. We confirmed that M. kondana is taxonomically distinct from M. meltada, and based on our estimates of its occurrence and occupancy, M. kondana continues to be treated as CR until further detailed investigations.
Acknowledgments
This work was supported by Mohamed bin Zayed Species Conservation Fund (UAE), CEPF-ATREE Western Ghats Small Grants Program, India and People’s Trust for Endangered Species (PTES), UK. We thank the National Centre for Biological Sciences (NCBS), Bengaluru for providing DNA sequencing facility. We are grateful to Maharashtra Forest Department for giving permission for this work. We thank Dr. Deepak Apte, Director; Dr. Asad Rahamani, Former Director; Rahul Khot, Assistant Director and Dr. Varad Giri, Former Curator of the BNHS for their support and encouragement throughout this project. We are grateful to the Natural History Collection Department, BNHS non-research staff Vithoba Hegade, Vinod Patil, Shyam Jadhav and Parshuram Parvate for their assistance. We also thank Ganesh Mane, Santhosh Kamble, Amol Lokhande, Sachin Patil, Mrugank Prabhu, Harish Kulkarni, Avinash Adsul, Gaurav Deshmane and Sandeep Jadhav for field assistance. We thank Mukta Joshi, Krishnapriya Tamma and Amruta Varudkar for assistance in DNA sequencing. We extend our gratitude to Santosh Dimble, Promod Mujumale, Vikas Mujumale and Vijay Mujumale for helping with local transport and lodging during fieldwork.
References
Adams, D.C., M.L. Collyer, A. Kaliontzopoulou and E. Sherratt. 2017. Geomorph: software for geometric morphometric analyses. R package version 3.0.5. https://cran.r-project.org/package=geomorph.Search in Google Scholar
Agrawal, V.C. 2000. Taxonomic studies on Indian Muridae and Hystricidae (Mammalia: Rodentia). Records of the Zoological Survey of India, Occasional Paper No. 180. Director, Zoological Survey of India, Calcutta. pp. 108–115.Search in Google Scholar
Aguirre-Gutiérrez, J., L.G. Carvalheiro, C. Polce, E.E. van Loon, N. Raes, M. Reemer and J.C. Biesmeijer. 2013. Fit-for-purpose: species distribution model performance depends on evaluation criteria – Dutch Hoverflies as a case study. PLoS One 8: 1–11.10.1371/journal.pone.0063708Search in Google Scholar
Anderson, R.P., A.T. Peterson and M. Gómez-Laverde. 2002. Using niche-based GIS modeling to test geographic predictions of competitive exclusion and competitive release in South American pocket mice. Oikos 98: 3–16.10.1034/j.1600-0706.2002.t01-1-980116.xSearch in Google Scholar
Bajaru, S.B. 2015. Distribution and assessment of the population status of Critically Endangered Kondana Soft-furred Rat, with a special emphasis on implementation of the conservation management plan at Sinhgad. Report submitted to Critical Ecosystem Partnership Fund (CEPF) – ATREE Western Ghats Small Grant Programme.Search in Google Scholar
Benson, D.A., M. Cavanaugh, K. Clark, I. Karsch-Mizrachi, D.J. Lipman, J. Ostell and E.W. Sayers. 2013. GenBank. Nucleic Acids Res. 41: D36–D42.10.1093/nar/gks1195Search in Google Scholar
Bookstein, F.L. 1991. Morphometric tools for landmark data. Cambridge University Press, Cambridge. pp. 435.Search in Google Scholar
Chandrahas, R.K. and A.K. Krishnaswami. 1974. Ecology of soft-furred Field Rat, Rattus meltada meltada (Gray) in Kolar Mysore state. J. Bombay Nat. Hist. Soc. 70: 447–457.Search in Google Scholar
Collyer, M.L., D.J. Sekora and D.C. Adams. 2015. A method for analysis of phenotypic change for phenotypes described by high-dimensional data. Heredity 115: 357–365.10.1038/hdy.2014.75Search in Google Scholar
Corbet, G.B. and J.E. Hill. 1992. The mammals of the Indomalayan region: a systematic review. Oxford University Press, Oxford, United Kingdom. pp. 45.Search in Google Scholar
Dauby, G. 2018. ConR: computation of parameters used in preliminary assessment of conservation status. R package version 1.2.2. https://CRAN.R-project.org/package=ConR.Search in Google Scholar
Dryden, I.L. and K.V. Mardia. 1998. Statistical shape analysis. John Wiley and Sons, Chichester. pp. 347.Search in Google Scholar
Ducroz, J.F., V. Volobouev and L. Granjon. 2001. An assessment of the systematics of arvicanthine rodents using mitochondrial DNA sequences: evolutionary and biogeographical implications. J. Mamm. Evol. 8: 173–206.10.1023/A:1012277012303Search in Google Scholar
Elith, J., C.H. Graham, R.P. Anderson, M. Dudík, S. Ferrier, A. Guisan, R.J. Hijmans, F. Huettmann, J.R. Leathwick, A. Lehmann, J. Li, L.G. Lohmann, B.A. Loiselle, G. Manion, C. Moritz, M. Nakamura, Y. Nakazawa, J.M. Overton, A.T. Peterson, S.J. Phillips, K. Richardson, R. Scachetti-Pereira, R.E. Schapire, J. Soberón, S. Williams, M.S. Wisz and N.E. Zimmermann. 2006. Novel methods improve prediction of species’ distributions from occurrence data. Ecography 29: 129–151.10.1111/j.2006.0906-7590.04596.xSearch in Google Scholar
Gupta, S., K. Mondal, K. Sankar and Q. Qureshi. 2013. Diversity and abundance of rodents in the semi-arid landscape of Sariska Tiger Reserve, Western India. J. Bombay Nat. Hist. Soc. 110: 122–128.Search in Google Scholar
Hernandez, P.A., C.H. Graham, L.L. Master and D.L. Albert. 2006. The effect of sample size and species characteristics on performance of different species distribution modeling methods. Ecography 29: 773–785.10.1111/j.0906-7590.2006.04700.xSearch in Google Scholar
Hijmans, R.J., S. Phillips, J. Leathwick and J. Elith. 2017. dismo: Species distribution modeling. R package version 1.1-4. https://CRAN.R-project.org/package=dismo.Search in Google Scholar
Kumar, S., G. Stecher and K. Tamura. 2016. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33: 1870–1874.10.1093/molbev/msw054Search in Google Scholar
Lanfear, R., P.B. Frandsen, A.M. Wright, T. Senfeld and B. Calcott. 2016. PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol. Biol. Evol. 34: 772–773.10.1093/molbev/msw260Search in Google Scholar
Lecompte, É., L. Granjon, J.K. Peterhans and C. Denys. 2002. Cytochrome b-based phylogeny of the Praomys group (Rodentia, Murinae): a new African radiation? C. R. Biol. 325: 827–840.10.1016/S1631-0691(02)01488-9Search in Google Scholar
Lecompte, E., C. Denys and L. Granjon. 2005. Confrontation of morphological and molecular data: the Praomys group (Rodentia, Murinae) as a case of adaptive convergences and morphological stasis. Mol. Phylogenetics Evol. 37: 899–919.10.1016/j.ympev.2005.06.018Search in Google Scholar
Lecompte, E., K. Aplin, C. Denys, F. Catzeflis, M. Chades and P. Chevret. 2008. Phylogeny and biogeography of African Murinae based on mitochondrial and nuclear gene sequences, with a new tribal classification of the subfamily. BMC Evol. Biol. 8: 199.10.1186/1471-2148-8-199Search in Google Scholar
Michaux, J., P. Chevret and S. Renaud. 2007. Morphological diversity of Old World rats and mice (Rodentia, Muridae) mandible in relation with phylogeny and adaptation. J. Zool. Syst. Evol. Res. 45: 263–279.10.1111/j.1439-0469.2006.00390.xSearch in Google Scholar
Mishra, A.C. and V. Dhanda. 1975. Review of the genus Millardia (Rodentia: Muridae), with description of a new species. J. Mammal. 56: 76–80.10.2307/1379607Search in Google Scholar
Molur, S. and M. Singh. 2009. Non-volant small mammals of the Western Ghats of Coorg District, southern India. JoTT 1: 589–608.10.11609/JoTT.o2330.589-608Search in Google Scholar
Mudappa, D., A. Kumar and R. Chellam. 2001. Abundance and habitat selection of the Malabar spiny dormouse in the rainforests of the southern Western Ghats, India. Curr. Sci. India 80: 424–427.Search in Google Scholar
Muscarella, R., P.J. Galante, M. Soley-Guardia, R.A. Boria, J. Kass, M. Uriarte and R.P. Anderson. 2014. ENMeval: an R package for conducting spatially independent evaluations and estimating optimal model complexity for ecological niche models. Methods Ecol. Evol. 5: 1198–1205.10.1111/2041-210X.12261Search in Google Scholar
Phillips, S.J., R.P. Anderson and R.E. Schapire. 2006. Maximum entropy modelling of species geographic distributions. Ecol. Model. 190: 231–259.10.1016/j.ecolmodel.2005.03.026Search in Google Scholar
Prabhakar. A. 1998. Small mammals of fragmented rainforests of the Western Ghats. Ph.D. Thesis, Bharaliyar University, India.Search in Google Scholar
Pradhan, M.S., S. Molur and P.O. Nameer. 2008. Millardia kondana. The IUCN Red List of Threatened Species. Version 2018. 1. <www.iucnredlist.org>. Accessed on 15 June 2018.Search in Google Scholar
Prakash, I. and P. Singh. 2005. Ecology of small mammals of desert and montane ecosystems. Scientific Publishers, Jodhpur, India. pp. 17–80.Search in Google Scholar
Prater, S.H. 1998. The book of Indian animals. Oxford University Press, India.Search in Google Scholar
Proosdij, A.S.J., M.S.M. Sosef, J.J. Wieringa and N. Raes. 2016. Minimum required number of specimen records to develop accurate species distribution models. Ecography 39: 542–552.10.1111/ecog.01509Search in Google Scholar
Ramchandran, V. 2013. Effect of habitat alteration on canopy bird and small mammal communities in the wet evergreen forests of the Western Ghats. Ph.D. Thesis, Manipal University, India.Search in Google Scholar
Rana, B.D. 1985. Ecological distribution of Rattus meltada in India. J. Bombay Nat. Hist. Soc. 85: 573–580.Search in Google Scholar
R Core Team. 2017. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.Search in Google Scholar
Rödder, D. and J.O. Engler. 2011. Quantitative metrics of over-laps in Grinnellian niches: advances and possible drawbacks. Global Ecol. Biogeogr. 20: 915–927.10.1111/j.1466-8238.2011.00659.xSearch in Google Scholar
Rohlf, F.J. 2017. tpsDig2, version 2.30. TpsSeries. Stony Brook: SUNY, Department of Ecology and Evolution. http://life.bio.sunysb.edu/morph/.Search in Google Scholar
Rohlf, F.J. and L.E. Marcus. 1993. A revolution in morphometrics. Trends. Ecol. Evol. 8: 129–132.10.1016/0169-5347(93)90024-JSearch in Google Scholar
Ronquist, F., M. Teslenko, P. Van Der Mark, D.L. Ayres, A. Darling, S. Hohna, B. Larget, L. Liu, M.A. Suchard and J.P. Huelsenbeck. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61: 539–542.10.1093/sysbio/sys029Search in Google Scholar PubMed PubMed Central
Safi, K., K. Armour-Marshall, J.E.M. Baillie and N.J.B. Isaac. 2013. Global patterns of evolutionary distinct and globally endangered amphibians and mammals. PLoS One 8: e63582.10.1371/journal.pone.0063582Search in Google Scholar PubMed PubMed Central
Schoener, T.W. 1970. Nonsynchronous spatial overlap of lizards in patchy habitats. Ecology 51: 408–418.10.2307/1935376Search in Google Scholar
Shanker, K. 2003. Small mammals in montane ecosystems of the Nilgiris, southern India: their ecology and natural history. J. Bombay Nat. Hist. Soc. 100: 46–57.Search in Google Scholar
Shenoy, K. and P.S. Madhusudan. 2006. Small mammal communities in a rapidly developing southern Indian city. Zoos Print J. 21: 2152–2159.10.11609/JoTT.ZPJ.1139.2152-9Search in Google Scholar
Sikes, R.S., W.L. Gannon and the Animal Care and Use Committee of the American Society of Mammalogists. 2011. Guidelines of the American Society of Mammalogists for the use of wild mammals in research. J. Mammal. 92: 235–253.10.1644/10-MAMM-F-355.1Search in Google Scholar
Silvestro, D. and I. Michalak. 2012. raxmlGUI: a graphical front-end for RaxML. Org. Divers. Evol. 12: 335–337.10.1007/s13127-011-0056-0Search in Google Scholar
Slice, D.E. 2007. Geometric morphometrics. Annu. Rev. Anthropol. 36: 261–281.10.1146/annurev.anthro.34.081804.120613Search in Google Scholar
Stamatakis, A. 2014. RaxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312–1313.10.1093/bioinformatics/btu033Search in Google Scholar PubMed PubMed Central
Steppan, J.S. and J.J. Schenk. 2017. Muroid rodent phylogenetics: 900-Species tree reveals increasing diversification rates. PLoS One 12: e0183070.10.1371/journal.pone.0183070Search in Google Scholar PubMed PubMed Central
Talmale, S.S. 2007. Studies on small mammal diversity in Maharashtra State. Ph.D. Thesis, University of Pune, India. pp. 431.Search in Google Scholar
Talmale, S.S., R. Tilak and M.S. Pradhan. 2013. Additional collection record of Sinhgarh Rat Millardia kondana Mishra and Dhanda from Sinhgarh, Pune, India. Records of Zoological Survey of India 113: 189–191.Search in Google Scholar
Venables, W.N. and B.D. Ripley. 2002. Modern applied statistics with S. Fourth Edition. Springer, New York. ISBN 0-387-95457-0.10.1007/978-0-387-21706-2Search in Google Scholar
Venkataraman, M., K. Shanker and R. Sukumar. 2005. Small mammal communities of tropical forest habitats in Mudumalai Wildlife Sanctuary, southern India. Mammalia 69: 349–358.10.1515/mamm.2005.028Search in Google Scholar
Wickham, H. 2009. ggplot2: Elegant graphics for data analysis. Springer-Verlag, New York.10.1007/978-0-387-98141-3Search in Google Scholar
Wieczorek, C. and J. Wieczorek. 2015. Georeferencing calculator (version 20160929). Museum of Vertebrate Zoology, University of California, Berkeley. http://manisnet.org/gci2.html. Accessed on 20 January 2018.Search in Google Scholar
Supplementary Material
The online version of this article offers supplementary material (https://doi.org/10.1515/mammalia-2019-0056).
©2020 Walter de Gruyter GmbH, Berlin/Boston