Assessing the status of critically endangered Kondana soft-furred rat (Millardia kondana) using integrative taxonomy: combining evidence from morphological, molecular and environmental niche modeling

Sameer B. Bajaru 1 , Aparna Lajmi 2 , 3 , Ranjit Manakadan 4 , Amol R. Kulavmode 4  and Uma Ramakrishnan 3
  • 1 Natural History Collection Department, Bombay Natural History Society, Hornbill House, S. B. S. Road, Fort, Mumbai 400001, India
  • 2 Institute of Evolution, Department of Evolutionary and Environmental Biology, University of Haifa, Haifa, Israel
  • 3 National Centre for Biological Sciences, Tata Institute of Fundamental Research, Bellary Road, Bangalore 560065, India
  • 4 Bombay Natural History Society, Hornbill House, S. B. S. Road, Fort, Mumbai 400001, India
Sameer B. Bajaru
  • Corresponding author
  • Natural History Collection Department, Bombay Natural History Society, Hornbill House, S. B. S. Road, Fort, Mumbai 400001, India
  • Email
  • Search for other articles:
  • degruyter.comGoogle Scholar
, Aparna Lajmi
  • Institute of Evolution, Department of Evolutionary and Environmental Biology, University of Haifa, Haifa, Israel
  • National Centre for Biological Sciences, Tata Institute of Fundamental Research, Bellary Road, Bangalore 560065, India
  • Search for other articles:
  • degruyter.comGoogle Scholar
, Ranjit Manakadan
  • Bombay Natural History Society, Hornbill House, S. B. S. Road, Fort, Mumbai 400001, India
  • Search for other articles:
  • degruyter.comGoogle Scholar
, Amol R. Kulavmode
  • Bombay Natural History Society, Hornbill House, S. B. S. Road, Fort, Mumbai 400001, India
  • Search for other articles:
  • degruyter.comGoogle Scholar
and Uma Ramakrishnan
  • National Centre for Biological Sciences, Tata Institute of Fundamental Research, Bellary Road, Bangalore 560065, India
  • Search for other articles:
  • degruyter.comGoogle Scholar

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.

  • 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.

  • 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.

  • 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.

  • 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.

    • Crossref
    • Export Citation
  • 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.

  • 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.

    • Crossref
    • Export Citation
  • Bookstein, F.L. 1991. Morphometric tools for landmark data. Cambridge University Press, Cambridge. pp. 435.

  • 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.

  • 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.

    • Crossref
    • PubMed
    • Export Citation
  • 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.

  • 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.

  • Dryden, I.L. and K.V. Mardia. 1998. Statistical shape analysis. John Wiley and Sons, Chichester. pp. 347.

  • 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.

    • Crossref
    • Export Citation
  • 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.

    • Crossref
    • Export Citation
  • 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.

  • 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.

    • Crossref
    • Export Citation
  • 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.

  • 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.

    • Crossref
    • PubMed
    • Export Citation
  • 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.

  • 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.

  • 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.

    • Crossref
    • Export Citation
  • 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.

    • Crossref
    • PubMed
    • Export Citation
  • 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.

    • Crossref
    • Export Citation
  • 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.

    • Crossref
    • Export Citation
  • Molur, S. and M. Singh. 2009. Non-volant small mammals of the Western Ghats of Coorg District, southern India. JoTT 1: 589–608.

  • 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.

  • 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.

    • Crossref
    • Export Citation
  • Phillips, S.J., R.P. Anderson and R.E. Schapire. 2006. Maximum entropy modelling of species geographic distributions. Ecol. Model. 190: 231–259.

    • Crossref
    • Export Citation
  • Prabhakar. A. 1998. Small mammals of fragmented rainforests of the Western Ghats. Ph.D. Thesis, Bharaliyar University, India.

  • 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.

  • Prakash, I. and P. Singh. 2005. Ecology of small mammals of desert and montane ecosystems. Scientific Publishers, Jodhpur, India. pp. 17–80.

  • Prater, S.H. 1998. The book of Indian animals. Oxford University Press, India.

  • 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.

    • Crossref
    • Export Citation
  • 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.

  • Rana, B.D. 1985. Ecological distribution of Rattus meltada in India. J. Bombay Nat. Hist. Soc. 85: 573–580.

  • R Core Team. 2017. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.

  • 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.

    • Crossref
    • Export Citation
  • Rohlf, F.J. 2017. tpsDig2, version 2.30. TpsSeries. Stony Brook: SUNY, Department of Ecology and Evolution. http://life.bio.sunysb.edu/morph/.

  • Rohlf, F.J. and L.E. Marcus. 1993. A revolution in morphometrics. Trends. Ecol. Evol. 8: 129–132.

    • Crossref
    • PubMed
    • Export Citation
  • 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.

    • Crossref
    • PubMed
    • Export Citation
  • 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.

    • Crossref
    • PubMed
    • Export Citation
  • Schoener, T.W. 1970. Nonsynchronous spatial overlap of lizards in patchy habitats. Ecology 51: 408–418.

    • Crossref
    • Export Citation
  • 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.

  • Shenoy, K. and P.S. Madhusudan. 2006. Small mammal communities in a rapidly developing southern Indian city. Zoos Print J. 21: 2152–2159.

    • Crossref
    • Export Citation
  • 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.

  • Silvestro, D. and I. Michalak. 2012. raxmlGUI: a graphical front-end for RaxML. Org. Divers. Evol. 12: 335–337.

    • Crossref
    • Export Citation
  • Slice, D.E. 2007. Geometric morphometrics. Annu. Rev. Anthropol. 36: 261–281.

    • Crossref
    • Export Citation
  • Stamatakis, A. 2014. RaxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312–1313.

    • Crossref
    • PubMed
    • Export Citation
  • Steppan, J.S. and J.J. Schenk. 2017. Muroid rodent phylogenetics: 900-Species tree reveals increasing diversification rates. PLoS One 12: e0183070.

    • Crossref
    • PubMed
    • Export Citation
  • Talmale, S.S. 2007. Studies on small mammal diversity in Maharashtra State. Ph.D. Thesis, University of Pune, India. pp. 431.

  • 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.

  • Venables, W.N. and B.D. Ripley. 2002. Modern applied statistics with S. Fourth Edition. Springer, New York. ISBN 0-387-95457-0.

  • 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.

  • Wickham, H. 2009. ggplot2: Elegant graphics for data analysis. Springer-Verlag, New York.

  • 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.

Purchase article
Get instant unlimited access to the article.
$42.00
Log in
Already have access? Please log in.


or
Log in with your institution

Journal + Issues

Mammalia is a peer-reviewed journal devoted to the inventory, analysis and interpretation of Mammalian diversity. It publishes original results on all aspects of systematics (comparative, functional and evolutionary morphology; morphometrics; phylogeny; biogeography; taxonomy and nomenclature), biology, ecology and conservation of mammals.

Search