Primates

, Volume 53, Issue 2, pp 157–170 | Cite as

First indications of a highland specialist among mouse lemurs (Microcebus spp.) and evidence for a new mouse lemur species from eastern Madagascar

  • Ute Radespiel
  • Jonah H. Ratsimbazafy
  • Solofonirina Rasoloharijaona
  • Herimalala Raveloson
  • Nicole Andriaholinirina
  • Romule Rakotondravony
  • Rose M. Randrianarison
  • Blanchard Randrianambinina
Original Article

Abstract

The factors that limit the distribution of the highly diverse lemur fauna of Madagascar are still debated. We visited an understudied region of eastern Madagascar, a lowland rainforest site (Sahafina, 29–230 m a.s.l.) close to the Mantadia National Park, in order to conduct a survey and collect further distributional data on mouse lemurs. We captured, measured, photographed, and sampled mouse lemurs from the Sahafina forest, performed standard phylogenetic methods based on three mitochondrial DNA genes, and conducted morphometric comparisons in order to clarify their phylogenetic position and taxonomic status. The mouse lemurs from the Sahafina forest could not be assigned to any of the known mouse lemur species and were highly divergent in all molecular analyses from all previously described species. Since they also differed morphometrically from their sister species and from their geographic neighbors, we propose species status and include a species description at the end. This study suggests that M. lehilahytsara may be the first highland specialist among all mouse lemurs. The distribution of the newly described mouse lemur is not fully known, but seems to be rather restricted and highly fragmented, which raises serious conservation concerns.

Keywords

Evolution Conservation Primates Taxonomy Phylogeny Morphometry 

Supplementary material

10329_2011_290_MOESM1_ESM.doc (340 kb)
Supplementary material 1 (DOC 340 kb)

References

  1. Andriantompohavana R, Zaonarivelo JR, Engberg SW, Randriamampionona R, McGuire SM, Shore GD, Rakotonomenjanahary R, Brenneman RA, Louis EE Jr (2006) Mouse lemurs of northwestern Madagascar with a description of a new species at Lokobe Special Reserve. Occas Pap Tex Tech Univ Mus 259:1–23Google Scholar
  2. Atsalis S (1999) Seasonal fluctuations in body fat and activity levels in a rain-forest species of mouse lemurs, Microcebus rufus. Int J Prim 20:883–910CrossRefGoogle Scholar
  3. Atsalis S, Schmid J, Kappeler PM (1996) Metrical comparisons of three species of mouse lemur. J Hum Evol 31:61–68CrossRefGoogle Scholar
  4. Cracraft J (1983) Species concepts and speciation analysis. Curr Ornithol 1:159–187Google Scholar
  5. Craul M, Zimmermann E, Rasoloharijaona S, Randrianambinina B, Radespiel U (2007) Unexpected species diversity of Malagasy primates (Lepilemur spp.) in the same biogeographical zone: a morphological and molecular approach with the description of two new species. BMC Evol Biol 7. doi:10.1186/1471-2148-7-83
  6. Dammhahn M, Kappeler PM (2005) Social system of Microcebus berthae, the world’s smallest primate. Int J Prim 26:407–435CrossRefGoogle Scholar
  7. Génin F (2008) Life in unpredictable environments: first investigation of the natural history of Microcebus griseorufus. Int J Prim 29:303–321CrossRefGoogle Scholar
  8. Goodman SM, Ganzhorn JU (2004) Biogeography of lemurs in the humid forests of Madagascar: the role of elevational distribution and rivers. J Biogeogr 31:47–55CrossRefGoogle Scholar
  9. Green GM, Sussman RW (1990) Deforestation history of the eastern rain forests of Madagascar from satellite images. Science 248:212–215PubMedCrossRefGoogle Scholar
  10. Groeneveld LF, Weisrock DW, Rasoloarison RM, Yoder AD, Kappeler PM (2009) Species delimitation in lemurs: multiple genetic loci reveal low levels of species diversity in the genus Cheirogaleus. BMC Evol Biol 9:30PubMedCrossRefGoogle Scholar
  11. Groeneveld LF, Rasoloarison RM, Kappeler PM (2011) Morphometrics confirm taxonomic deflation in dwarf lemurs (Primates: Cheirogaleidae), as suggested by genetics. Zool J Linn Soc 161:229–244CrossRefGoogle Scholar
  12. Guschanski K, Olivieri G, Funk SM, Radespiel U (2007) MtDNA reveals strong genetic differentiation among geographically isolated populations of the golden brown mouse lemur, Microcebus ravelobensis. Conserv Genet 8:809–821CrossRefGoogle Scholar
  13. Hafen T, Neveu H, Rumpler Y, Wilden I, Zimmermann E (1998) Acoustically dimorphic advertisement calls separate morphologically and genetically homogenous populations of the grey mouse lemur (Microcebus murinus). Folia Primatol 69(Suppl 1):342–356PubMedCrossRefGoogle Scholar
  14. Harper GJ, Steininger MK, Tucker CJ, Juhn D, Hawkins F (2007) Fifty years of deforestation and forest fragmentation in Madagascar. Env Cons 34:1–9CrossRefGoogle Scholar
  15. Kamilar JM, Muldoon KM (2010) The climatic niche diversity of Malagasy primates: a phylogenetic perspective. PLoS ONE 5:e11073PubMedCrossRefGoogle Scholar
  16. Kappeler PM, Rasoloarison RM, Razafimanantsoa L, Walter L, Roos C (2005) Morphology, behaviour and molecular evolution of giant mouse lemurs (Mirza spp.) Gray, 1870, with description of a new species. Primate Rep 71:3–26Google Scholar
  17. Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163PubMedCrossRefGoogle Scholar
  18. Louis EE Jr, Coles MS, Andriantompohavana R, Sommer JA, Engberg SE, Zaonarivelo JR, Mayor MI, Brenneman RA (2006) Revision of the mouse lemurs (Microcebus) of Eastern Madagascar. Int J Primatol 27:347–389CrossRefGoogle Scholar
  19. Louis EE Jr, Engberg SE, McGuire SM, McCormick MJ, Randriamampionona R, Ranaivoarisoa JF, Bailey CA, Mittermeier RA, Lei R (2008) Revision of the mouse lemurs, Microcebus (Primates, Lemuriformes), of northern and northwestern Madagascar with descriptions of two new species at Montagne d’Ambre National Park and Antafondro classified forest. Primate Conserv 23:19–38CrossRefGoogle Scholar
  20. Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring HarborGoogle Scholar
  21. Mittermeier RA, Ganzhorn JU, Konstant WR, Glander K, Tattersall I, Groves CP, Rylands AB, Hapke A, Ratsimbazafy J, Mayor MI, Louis EE Jr, Rumpler Y, Schwitzer C, Rasoloarison RM (2008) Lemur diversity in Madagascar. Int J Primatol 29:1607–1656CrossRefGoogle Scholar
  22. Mittermeier RA, Louis EE Jr, Richardson M, Schwitzer C, Langrand O, Rylands AB, Hawkins F, Rajaobelina S, Ratsimbazafy J, Rasoloarison R, Roos C, Kappeler PM, Mackinnon J (2010) Lemurs of Madagascar, 3rd edn. Conservation International, ArlingtonGoogle Scholar
  23. Muldoon KM, Goodman SM (2010) Ecological biogeography of Malagasy non-volant mammals: community structure is correlated with habitat. J Biogeogr 37:1144–1159CrossRefGoogle Scholar
  24. Olivieri G, Zimmermann E, Randrianambinina B, Rasoloharijaona S, Rakotondravony D, Guschanski K, Radespiel U (2007) The ever-increasing diversity in mouse lemurs: three new species in north and northwestern Madagascar. Mol Phylogenet Evol 43:309–327PubMedCrossRefGoogle Scholar
  25. Olivieri GL, Sousa V, Chikhi L, Radespiel U (2008) From genetic diversity and structure to conservation: genetic signature of recent population declines in three mouse lemur species (Microcebus spp.). Biol Conserv 141:1257–1271CrossRefGoogle Scholar
  26. Padial JM, Miralles A, De la Riva I, Vences M (2010) The integrative future of taxonomy. Front Zool 7:16. doi:10.1186/1742-9994-7-16 PubMedCrossRefGoogle Scholar
  27. Pearson RG, Raxworthy CJ (2009) The evolution of local endemism in Madagascar: watershed versus climatic gradient hypotheses evaluated by null biogeographic models. Evolution 63:959–967PubMedCrossRefGoogle Scholar
  28. Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818PubMedCrossRefGoogle Scholar
  29. Radespiel U, Olivieri G, Rasolofoson DW, Rakotondratsimba G, Rakotonirainy O, Rasoloharijaona S, Randrianambinina B, Ratsimbazafy JH, Ratelolahy F, Randriamboavonjy T, Rasolofoharivelo T, Craul M, Rakotozafy L, Randrianarison RM (2008) Exceptional diversity of mouse lemurs (Microcebus spp.) in the Makira region with the description of one new species. Am J Primatol 70:1033–1046PubMedCrossRefGoogle Scholar
  30. Randrianambinina B (2001) Contribution à l’étude comparative de l’écoéthologie de deux microcèbes rouges de Madagascar: Microcebus ravelobensis (Zimmermann et al., 1998) Microcebus rufus (Lesson, 1840) (doctoral thesis). University of Antananarivo, MadagascarGoogle Scholar
  31. Rasoloarison RM, Goodman SM, Ganzhorn JU (2000) Taxonomic revision of mouse lemurs (Microcebus) in the western portions of Madagascar. Int J Primatol 21:963–1019CrossRefGoogle Scholar
  32. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574PubMedCrossRefGoogle Scholar
  33. Seutin G, White BN, Boag PT (1991) Preservation of avian blood and tissue samples for DNA analysis. Can J Zool 69:82–90CrossRefGoogle Scholar
  34. Silvestro D, Michalak (2010) raxmlGUI: a graphical front-end for RAxML. http://sourceforge.net/projects/raxmlgui/
  35. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690PubMedCrossRefGoogle Scholar
  36. Tattersall I (2007) Madagascar's lemurs: cryptic diversity or taxonomic inflation? Evol Anthropol 16:12–23Google Scholar
  37. Thalmann O, Hebler J, Poinar HN, Pääbo S, Vigilant L (2004) Unreliable mtDNA data due to nuclear insertions: a cautionary tale from analysis of humans and other great apes. Mol Ecol 13:321–335PubMedCrossRefGoogle Scholar
  38. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882PubMedCrossRefGoogle Scholar
  39. Vences M, Wollenberg KC, Vieites DR, Lees DC (2009) Madagascar as a model region of species diversification. Trends Ecol Evol 24:456–465PubMedCrossRefGoogle Scholar
  40. Weisrock DW, Rasoloarison RM, Fiorentino L, Ralison JM, Goodman SM, Kappeler PM, Yoder AD (2010) Delimiting species without nuclear monophyly in Madagascar’s mouse lemurs. PLoS ONE 5:e9883. doi:10.1371/journal.pone.0009883 PubMedCrossRefGoogle Scholar
  41. Wilmé L, Goodman SM, Ganzhorn JU (2006) Biogeographic evolution of Madagascar’s microendemic biota. Science 312:1063–1065PubMedCrossRefGoogle Scholar
  42. Yoder AD, Rasoloarison RM, Goodman SM, Irwin JA, Atsalis S, Ravosa MJ, Ganzhorn JU (2000) Remarkable species diversity in Malagasy mouse lemurs (primates, Microcebus). Proc Natl Acad Sci USA 97:11325–11330PubMedCrossRefGoogle Scholar
  43. Zimmermann E, Cepok S, Rakotoarison N, Zietemann V, Radespiel U (1998) Sympatric mouse lemurs in North-West Madagascar: a new rufous mouse lemur species (Microcebus ravelobensis). Folia Primatol 69:106–114PubMedCrossRefGoogle Scholar

Copyright information

© Japan Monkey Centre and Springer 2011

Authors and Affiliations

  • Ute Radespiel
    • 1
    • 2
  • Jonah H. Ratsimbazafy
    • 2
    • 3
  • Solofonirina Rasoloharijaona
    • 2
    • 4
  • Herimalala Raveloson
    • 2
    • 4
  • Nicole Andriaholinirina
    • 2
    • 4
  • Romule Rakotondravony
    • 2
    • 4
  • Rose M. Randrianarison
    • 2
  • Blanchard Randrianambinina
    • 2
    • 4
  1. 1.Institute of ZoologyUniversity of Veterinary Medicine HannoverHannoverGermany
  2. 2.Groupe d’étude et de recherche sur les Primates de Madagascar (GERP)AntananarivoMadagascar
  3. 3.Durrell Wildlife Conservation Trust-MadagascarAntananarivoMadagascar
  4. 4.Faculté des SciencesUniversité de MahajangaMahajangaMadagascar

Personalised recommendations