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International Journal of Primatology

, Volume 36, Issue 6, pp 1132–1153 | Cite as

Genetic Diversity, Population Size, and Conservation of the Critically Endangered Perrier’s Sifaka (Propithecus perrieri)

  • Jordi SalmonaEmail author
  • Helena Teixeira
  • Emmanuel Rasolondraibe
  • Isa Aleixo-Pais
  • Célia Kun-Rodrigues
  • Ando Nantenaina Rakotonanahary
  • Fabien Jan
  • Clément Joseph Rabarivola
  • John Rigobert Zaonarivelo
  • Nicole Volasoa Andriaholinirina
  • Lounès ChikhiEmail author
Article

Abstract

Genetic data can be combined with ecological data to study the demographic history of a species, identify landscape features that influence migration patterns, and guide conservation efforts. Perrier’s sifaka (Propithecus perrieri) is a Critically Endangered, rare, and elusive social lemur living in a very restricted, fragmented landscape. To assess the effect of habitat loss and fragmentation on the genetic diversity of the Perrier’s sifaka population we examined 24 microsatellite markers genotyped for 67 samples corresponding to 42 individuals. Perrier’s sifaka shows a low current effective population size (ca. 52–105) and a strong heterozygosity excess, suggesting a historically large but dwindling population. Moreover, we identified a pattern of isolation by distance, typical of continuous habitat, suggesting that sifakas were still able to cross the grasslands between forest fragments in the recent past. Our study calls for a unified conservation plan covering the two protected areas where the species is still present, if not the whole area of its past distribution. Further studies inferring the past demographic history of Perrier’s sifaka may confirm the population decline and shed light on its potential causes.

Keywords

Bottleneck Indriidae Lemur Madagascar Strepsirrhini 

Notes

Acknowledgments

We thank CAFF/CORE, the Direction Générale de l’Environnement et des Forêts, Madagascar National Park, the Fanamby NGO (in particular S. Rajaobelina V. Rasoloarison, P. Ranirison, and S. Wohlhauser), the Direction Régionale de l’Environnement et des Forêts région DIANA, and M. Banks for discussion and advices on Perrier’s sifaka. The field work was possible thanks to the continuous support of the Département de Biologie Animale et Ecologie, University of Mahajanga; the University of Antsiranana; and to a large extent, thanks to the participation of many great local guides and cooks whom we warmly thank for their help in the field and for sharing their incomparable expertise of the forest, Misaotra anareo jiaby. Finally we thank the Genomics Unit at the IGC, Sequencing Service, for their collaboration and L. Wilmé, R. Heller, E. Quéméré, and I. Carvalho for comments and discussion on the manuscript, Joanna Setchell and the editors of Biological Conservation and American Journal of Primatology as well as several anonymous reviewers who substantially helped improving the manuscript. Financial support for this study was provided by the Fundação para a Ciência e a Tecnologia (PTDC/BIA-BEC/100176/2008, PTDC/BIA-BIC/4476/2012, and SFRH/BD/64875/2009); the GDRI Madagascar; the Laboratoire d’Excellence (LABEX) entitled TULIP (ANR-10-LABX-41); the Rufford Small Grant Foundation, grant 10941-1; and the Instituto Gulbenkian de Ciência. C. Kun-Rodrigues and H. Teixeira were funded by an Optimus!Alive-IGC fellowship. This study was conducted in agreement with the laws of the countries of Portugal, France, and Madagascar.

Supplementary material

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References

  1. Agudo, R., Rico, C., Vilà, C., Hiraldo, F., & Donázar, J. A. (2010). The role of humans in the diversification of a threatened island raptor. BMC Evolutionary Biology, 10(1), 384.PubMedPubMedCentralCrossRefGoogle Scholar
  2. Allcock, A. L., & Strugnell, J. M. (2012). Southern Ocean diversity: new paradigms from molecular ecology. Trends in Ecology & Evolution, 27(9), 520–528.CrossRefGoogle Scholar
  3. Allentoft, M. E., Heller, R., Oskam, C. L., Lorenzen, E. D., Hale, M. L., Gilbert, M. T. P., et al. (2014). Extinct New Zealand megafauna were not in decline before human colonization. Proceedings of the National Academy of Sciences of the USA, 111(13), 4922–4927.PubMedPubMedCentralCrossRefGoogle Scholar
  4. Allnutt, T. F., Ferrier, S., Manion, G., Powell, G. V., Ricketts, T. H., Fisher, B. L., et al. (2008). A method for quantifying biodiversity loss and its application to a 50-year record of deforestation across Madagascar. Conservation Letters, 1(4), 173–181.CrossRefGoogle Scholar
  5. Andren, H. (1994). Effects of habitat fragmentation on birds and mammals in landscapes with different proportions of suiTable habitat: a review. Oikos, 71(3), 355–366.CrossRefGoogle Scholar
  6. Asner, G. P., Rudel, T. K., Aide, T. M., Defries, R., & Emerson, R. (2009). A contemporary assessment of change in humid tropical forests. Conservation Biology, 23(6), 1386–1395.PubMedCrossRefGoogle Scholar
  7. Baden, A. L., Holmes, S. M., Johnson, S. E., Engberg, S. E., Louis, E. E., & Bradley, B. J. (2014). Species-level view of population structure and gene flow for a critically endangered primate (Varecia variegata). Ecology and Evolution, 4(13), 2675–2692.PubMedPubMedCentralCrossRefGoogle Scholar
  8. Banks, M. A. (2013). Determinants of abundance and the distribution of primates in northern Madagascar (Physical Anthropology). Ph.D. thesis, Stony Brook University.Google Scholar
  9. Banks, M. A., Ellis, E. R., & Wright, P. C. (2007). Global population size of a critically endangered lemur, Perrier’s sifaka. Animal Conservation, 10(2), 254–262.CrossRefGoogle Scholar
  10. Barrett, M. A., Brown, J. L., Morikawa, M. K., Labat, J.-N., & Yoder, A. D. (2010). CITES designation for endangered rosewood in Madagascar. Science, 328(5982), 1109–1110.PubMedCrossRefGoogle Scholar
  11. Belkhir, K., Borsa, P., Chikhi, L., Raufaste, N., & Catch, F. (2004). GENETIX 4. 0. 5. 2., Software under Windows™ for the genetics of the populations. Laboratory Genome, Populations, Interactions, CNRS UMR.Google Scholar
  12. Berec, L., Angulo, E., & Courchamp, F. (2007). Multiple Allee effects and population management. Trends in Ecology & Evolution, 22(4), 185–191.CrossRefGoogle Scholar
  13. Brenneman, R. A., Johnson, S. E., Bailey, C. A., Ingraldi, C., Delmore, K. E., Wyman, T. M., et al. (2012). Population genetics and abundance of the Endangered grey-headed lemur Eulemur cinereiceps in south-east Madagascar: assessing risks for fragmented and continuous populations. Oryx, 46(02), 298–307.CrossRefGoogle Scholar
  14. Buckland, S. T. (2001). Introduction to distance sampling: Estimating abundance of biological populations. New York: Oxford University Press.Google Scholar
  15. Buckland, S. T., Plumptre, A. J., Thomas, L., & Rexstad, E. A. (2010). Design and analysis of line transect surveys for primates. International Journal of Primatology, 31(5), 833–847.CrossRefGoogle Scholar
  16. Burivalova, Z. (2011). Remote sensing of vegetation in conservation: A case study from the dry and transitional forests of Andrafiamena, northern Madagascar. Master’s dissertation, Universite de Geneve and Conservatoire et Jardin botaniques de la Ville de Geneve, Genève.Google Scholar
  17. Carret, J.-C. (2013). Madagascar - Country Environmental Analysis (CEA): Taking stock and moving forward (No. 77993, pp. 1–164). The World Bank. http://documents.worldbank.org/curated/en/2013/05/17759163/madagascar-country-environmental-analysis-cea-taking-stock-moving-forward. Accessed 7 Nov 2014.
  18. Chikhi, L., Sousa, V. C., Luisi, P., Goossens, B., & Beaumont, M. A. (2010). The confounding effects of population structure, genetic diversity and the sampling scheme on the detection and quantification of population size changes. Genetics, 186(3), 983.PubMedPubMedCentralCrossRefGoogle Scholar
  19. Cornuet, J. M., & Luikart, G. (1996). Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics, 144(4), 2001.PubMedPubMedCentralGoogle Scholar
  20. Craul, M., Chikhi, L., Sousa, V., Olivieri, G. L., Rabesandratana, A., Zimmermann, E., & Radespiel, U. (2009). Influence of forest fragmentation on an endangered large-bodied lemur in northwestern Madagascar. Biological Conservation, 142, 2862--2871.Google Scholar
  21. Csilléry, K., Blum, M. G., Gaggiotti, O. E., & François, O. (2010). Approximate Bayesian computation (ABC) in practice. Trends in Ecology & Evolution, 25(7), 410–418.CrossRefGoogle Scholar
  22. Cushman, S. A., Wasserman, T. N., Landguth, E. L., & Shirk, A. J. (2013). Re-evaluating causal modeling with Mantel tests in landscape genetics. Diversity, 5(1), 51–72.CrossRefGoogle Scholar
  23. Dewar, R. E., Radimilahy, C., Wright, H. T., Jacobs, Z., Kelly, G. O., & Berna, F. (2013). Stone tools and foraging in northern Madagascar challenge Holocene extinction models. Proceedings of the National Academy of Sciences of the USA, 110(31), 12583–12588.PubMedPubMedCentralCrossRefGoogle Scholar
  24. Fahrig, L. (2003). Effects of habitat fragmentation on biodiversity. Annual Review of Ecology, Evolution, and Systematics, 34, 487–515.CrossRefGoogle Scholar
  25. Falush, D., Stephens, M., & Pritchard, J. K. (2007). Inference of population structure using multilocus genotype data: dominant markers and null alleles. Molecular Ecology Notes, 7(4), 574–578.PubMedPubMedCentralCrossRefGoogle Scholar
  26. Frankham, R., Briscoe, D. A., & Ballou, J. D. (2002). Introduction to conservation genetics (p. 619). Cambridge: Cambridge University Press.Google Scholar
  27. Frankham, R., Bradshaw, C. J., & Brook, B. W. (2014). Genetics in conservation management: revised recommendations for the 50/500 rules, Red List criteria and population viability analyses. Biological Conservation, 170, 56–63.CrossRefGoogle Scholar
  28. Franklin, I. R. (1980). Evolutionary change in small populations. Conservation biology: An evolutionary-ecological perspective (pp. 135–149). Sunderland, MA: Sinauer Associates.Google Scholar
  29. Frantz, A. C., Pope, L. C., Carpenter, P. J., Roper, T. J., Wilson, G. J., Delahay, R. J., & Burke, T. (2003). Reliable microsatellite genotyping of the Eurasian badger (Meles meles) using faecal DNA. Molecular Ecology, 12(6), 1649–1661.PubMedCrossRefGoogle Scholar
  30. Ganzhorn, J. U., Lowry, P. P., Schatz, G. E., & Sommer, S. (2001). The biodiversity of Madagascar: one of the world’s hottest hotspots on its way out. Oryx, 35(4), 346–348.CrossRefGoogle Scholar
  31. Gibson, L., Lee, T. M., Koh, L. P., Brook, B. W., Gardner, T. A., Barlow, J., et al. (2011). Primary forests are irreplaceable for sustaining tropical biodiversity. Nature, 478(7369), 378–381.PubMedCrossRefGoogle Scholar
  32. Global Witness. (2009). Investigation into the illegal felling, transport and export of precious wood in SAVA Region Madagascar. London: Environmental Investigation Agency.Google Scholar
  33. Godfrey, L. R., Jungers, W. L., Simons, E. L., Chatrath, P. S., & Rakotosamimanana, B. (1996). Past and present distributions of lemurs in Madagascar. In New directions in lemur studies (pp. 19–53). New York: Springer-Verlag.  10.1007/978-1-4615-4705-1_2 Accessed 26 March 2015.
  34. Gommery, D., Ramanivosoa, B., Faure, M., Guerin, C., Kerloc’h, P., Senegas, F., & Randrianantenaina, H. (2011). Oldest evidence of human activities in Madagascar on subfossil hippopotamus bones from Anjohibe (Mahajanga Province). Comptes Rendus Palevol, 10(4), 271–278.CrossRefGoogle Scholar
  35. Goodman, S. M., & Benstead, J. P. (2005). Updated estimates of biotic diversity and endemism for Madagascar. Oryx, 39(01), 73–77.CrossRefGoogle Scholar
  36. Goodman, S. M., & Wilmé, L. (2006a). Inventaires de la faune et de la flore du nord de Madagascar dans la région Loky-Manambato, Analamerana et Andavakoera. Recherche pour le Developement, 23, 238.Google Scholar
  37. Goodman, S. M., & Wilmé, L. (2006b). Introduction. Inventaires de la faune et de la flore du nord de Madagascar dans la région Loky-Manambato, Analamerana et Andavakoera. Recherche pour le Developement, 23, 1–36.Google Scholar
  38. Harper, G. J., Steininger, M. K., Tucker, C. J., Juhn, D., & Hawkins, F. (2007). Fifty years of deforestation and forest fragmentation in Madagascar. Environmental Conservation, 34(4), 325–333.CrossRefGoogle Scholar
  39. Hawkins, A. F. A., Chapman, P., Ganzhorn, J. U., Bloxam, Q. M. C., Barlow, S. C., & Tonge, S. J. (1990). Vertebrate conservation in Ankarana special reserve, northern Madagascar. Biological Conservation, 54(2), 83–110.CrossRefGoogle Scholar
  40. Heller, R., Chikhi, L., & Siegismund, H. R. (2013). The confounding effect of population structure on Bayesian skyline plot inferences of demographic history. PLoS ONE, 8(5), e62992.PubMedPubMedCentralCrossRefGoogle Scholar
  41. Hewitt, G. (2000). The genetic legacy of the Quaternary ice ages. Nature, 405(6789), 907–913.PubMedCrossRefGoogle Scholar
  42. Hewitt, G. M. (2004). Genetic consequences of climatic oscillations in the Quaternary. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 359(1442), 183–195.PubMedPubMedCentralCrossRefGoogle Scholar
  43. Hochachka, W. M., Martin, K., Doyle, F., & Krebs, C. J. (2000). Monitoring vertebrate populations using observational data. Canadian Journal of Zoology, 78(4), 521–529.CrossRefGoogle Scholar
  44. Humbert, H., Darne, G. C., & Besairie, H. (1965). Notice de la carte Madagascar. Institut Français de Pondichéry. http://library.wur.nl/WebQuery/clc/1939325. Accessed 6 Nov 2014.
  45. Irwin, M. T., Johnson, S. E., & Wright, P. C. (2005). The state of lemur conservation in south-eastern Madagascar: population and habitat assessments for diurnal and cathemeral lemurs using surveys, satellite imagery and GIS. Oryx, 39(2), 204–218.CrossRefGoogle Scholar
  46. IUCN, S. S. C. (2001). IUCN Red List categories and criteria: version 3.1. Prepared by the IUCN Species Survival Commission.Google Scholar
  47. IUCN (2014). 2014 IUCN Red List of threatened species, version 2014.2. http://www.iucnredlist.org/. Accessed 26 Nov 2015.
  48. Jacobson, B., & Peres-Neto, P. R. (2010). Quantifying and disentangling dispersal in metacommunities: how close have we come? How far is there to go? Landscape Ecology, 25(4), 495–507.CrossRefGoogle Scholar
  49. Jenkins, R. K. B., Keane, A., Rakotoarivelo, A. R., Rakotomboavonjy, V., Randrianandrianina, F. H., Razafimanahaka, H. J., et al. (2011). Analysis of patterns of bushmeat consumption reveals extensive exploitation of protected species in eastern Madagascar. PLoS ONE, 6(12), e27570.PubMedPubMedCentralCrossRefGoogle Scholar
  50. Jeppsson, T., & Forslund, P. (2012). Can life history predict the effect of demographic stochasticity on extinction risk? The American Naturalist, 179(6), 706–720.PubMedCrossRefGoogle Scholar
  51. Jombart, T., & Ahmed, I. (2011). adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics, 27(21), 3070–3071.PubMedPubMedCentralCrossRefGoogle Scholar
  52. Jungers, W. L., Godfrey, L. R., Simons, E. L., & Chatrath, P. S. (1995). Subfossil Indri indri from the Ankarana Massif of northern Madagascar. American Journal of Physical Anthropology, 97(4), 357–366.PubMedCrossRefGoogle Scholar
  53. Kalinowski, S. T. (2005). hp-rare 1.0: a computer program for performing rarefaction analysis on measures of allelic richness. Molecular Ecology Notes, 5(1), 187–189.CrossRefGoogle Scholar
  54. Kappeler, P. M., & Schäffler, L. (2008). The lemur syndrome unresolved: extreme male reproductive skew in sifakas (Propithecus verreauxi), a sexually monomorphic primate with female dominance. Behavioral Ecology and Sociobiology, 62(6), 1007–1015.CrossRefGoogle Scholar
  55. Keller, L. F., & Waller, D. M. (2002). Inbreeding effects in wild populations. Trends in Ecology & Evolution, 17(5), 230–241.CrossRefGoogle Scholar
  56. Khasin, M., Meerson, B., Khain, E., & Sander, L. M. (2012). Minimizing the population extinction risk by migration. Physical Review Letters, 109(13), 138104.PubMedCrossRefGoogle Scholar
  57. Kimura, M., & Ohta, T. (1969). The average number of generations until fixation of a mutant gene in a finite population. Genetics, 61(3), 763.PubMedPubMedCentralGoogle Scholar
  58. Kliman, R., Sheehy, B., & Schultz, J. (2008). Genetic drift and effective population size. Nature Education, 1(3), 3.Google Scholar
  59. Kramer, A. M., Dennis, B., Liebhold, A. M., & Drake, J. M. (2009). The evidence for Allee effects. Population Ecology, 51(3), 341–354.CrossRefGoogle Scholar
  60. Kun-Rodrigues, C., Salmona, J., Besolo, A., Rasolondraibe, E., Rabarivola, C., Marques, T. A., & Chikhi, L. (2014). New density estimates of a threatened sifaka species (Propithecus coquereli) in Ankarafantsika National Park. American Journal of Primatology, 76(6), 515–528.PubMedCrossRefGoogle Scholar
  61. Lande, R. (1993). Risks of population extinction from demographic and environmental stochasticity and random catastrophes. The American Naturalist, 142, 911–927.Google Scholar
  62. Laurance, W. F., Useche, D. C., Rendeiro, J., Kalka, M., Bradshaw, C. J., Sloan, S. P., et al. (2012). Averting biodiversity collapse in tropical forest protected areas. Nature, 489(7415), 290–294.PubMedCrossRefGoogle Scholar
  63. Lawler, R. R., Richard, A. F., & Riley, M. A. (2001). Characterization and screening of microsatellite loci in a wild lemur population (Propithecus verreauxi verreauxi). American Journal of Primatology, 55(4), 253–259.PubMedCrossRefGoogle Scholar
  64. Lawler, R. R., Caswell, H., Richard, A. F., Ratsirarson, J., Dewar, R. E., & Schwartz, M. (2009). Demography of Verreaux’s sifaka in a stochastic rainfall environment. Oecologia, 161(3), 491–504.PubMedCrossRefGoogle Scholar
  65. Lehman, S. M., & Mayor, M. (2004). Dietary patterns in Perrier’s sifakas (Propithecus diadema perrieri): a preliminary study. American Journal of Primatology, 62(2), 115–122.PubMedCrossRefGoogle Scholar
  66. Lei, R., Day, S., Ramarokoto, R., Shore, G. D., Louis, J., Edward, E., & Brenneman, R. A. (2008). Characterization of 21 microsatellites developed from Propithecus deckeni deckeni. Molecular Ecology Resources, 8(4), 773–776.PubMedCrossRefGoogle Scholar
  67. Luikart, G., & Cornuet, J.-M. (1998). Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conservation Biology, 12(1), 228–237.CrossRefGoogle Scholar
  68. Lynch, M., & Ritland, K. (1999). Estimation of pairwise relatedness with molecular markers. Genetics, 152(4), 1753–1766.PubMedPubMedCentralGoogle Scholar
  69. Manel, S., & Holderegger, R. (2013). Ten years of landscape genetics. Trends in Ecology & Evolution, 28(10), 614–621.CrossRefGoogle Scholar
  70. Mayor, M., & Lehman, S. M. (1999). Conservation of Perrier’s sifaka (Propithecus diadema perrieri) in Analamera Special Reserve, Madagascar. Lemur News, 4, 21–23.Google Scholar
  71. Mayor, M. I., Sommer, J. A., Huebinger, R. M., Barber, R. C., & Louis, E. E. (2002). Characterization of seven microsatellite marker loci in a genus of Malagasy lemurs (Propithecus). Molecular Ecology Notes, 2(4), 385–388.CrossRefGoogle Scholar
  72. Mazet, O., Rodríguez, W., & Chikhi, L. (2015). Demographic inference using genetic data from a single individual: separating population size variation from population structure. Theoretical Population Biology, 104, 46–58.PubMedCrossRefGoogle Scholar
  73. McGuire, S. M., Emodi, G. P., Shore, G. D., Brenneman, R. A., & Louis, E. E. (2009). Characterization of 21 microsatellite marker loci in the silky sifaka (Propithecus candidus). Conservation Genetics, 10(4), 985–988.CrossRefGoogle Scholar
  74. Meyers, D. M., & Ratsirarson, J. (1989). Distribution and conservation of two endangered sifakas in northern Madagascar. Primate Conservation, 10, 81–86.Google Scholar
  75. Meyers, D. M., & Wright, P. C. (1993). Resource tracking: Food availability and Propithecus seasonal reproduction. In J. Ganzhorn & P. M. Kappeler (Eds.), Lemur social systems and their ecological basis (pp. 179–192). New York: Plenum Press.CrossRefGoogle Scholar
  76. Minten, B., Randrianarisoa, J.-C., Randrianarison, L., & Food, C. (2003). Agriculture, pauvreté rurale et politiques économiques à Madagascar. Cornell Food and Nutrition Policy Program. http://www.hayzara.org/index.php/eng/content/download/496/4084/version/2/file/2003+-+Agriculture+pauvret%C3%A9+rurale+et+Politiques+Economiques+a+Madagascar.pdf Accessed 7 Nov 2014.
  77. Mitchell, M. W., Locatelli, S., Clee, P. R. S., Thomassen, H. A., & Gonder, M. K. (2015). Environmental variation and rivers govern the structure of chimpanzee genetic diversity in a biodiversity hotspot. BMC Evolutionary Biology, 15(1), 1.PubMedPubMedCentralCrossRefGoogle Scholar
  78. Mittermeier, R. A., Louis, E. E., Richardson, M., Schwitzer, C., Langrand, O., Rylands, A., et al. (2010). Lemurs of Madagascar (3rd ed.). Washington, DC: Conservation International.Google Scholar
  79. Moat, J., & Smith, P. (2007). Atlas of the vegetation of Madagascar/ Vegetation/atlas de la vegetation de Madagascar (Royal Botanic Gardens Kew). Kew Publishing. http://tna.europarchive.org/20080612120511/http://kew.org/publications/vegatlas_ai.doc. Accessed 25 Nov 2013.
  80. Morris, W. F., Altmann, J., Brockman, D. K., Cords, M., Fedigan, L. M., Pusey, A. E., et al. (2011). Low demographic variability in wild primate populations: fitness impacts of variation, covariation, and serial correlation in vital rates. The American Naturalist, 177(1), E14.PubMedPubMedCentralCrossRefGoogle Scholar
  81. Munson, L., Brown, J. L., Bush, M., Packer, C., Janssen, D., Reiziss, S. M., & Wildt, D. E. (1996). Genetic diversity affects testicular morphology in free-ranging lions (Panthera leo) of the Serengeti Plains and Ngorongoro Crater. Journal of Reproduction and Fertility, 108(1), 11–15.PubMedCrossRefGoogle Scholar
  82. Myers, N., Mittermeier, R. A., Mittermeier, C. G., Da Fonseca, G. A., & Kent, J. (2000). Biodiversity hotspots for conservation priorities. Nature, 403(6772), 853–858.PubMedCrossRefGoogle Scholar
  83. Nei, M. (1978). Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics, 89(3), 583.PubMedPubMedCentralGoogle Scholar
  84. Nikolic, N., & Chevalet, C. (2014). Detecting past changes of effective population size. Evolutionary Applications, 7(6), 663–681.PubMedPubMedCentralCrossRefGoogle Scholar
  85. Nunney, L., & Campbell, K. A. (1993). Assessing minimum viable population size: demography meets population genetics. Trends in Ecology & Evolution, 8(7), 234–239.CrossRefGoogle Scholar
  86. Olivieri, G. L., 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.). Biological Conservation, 141(5), 1257–1271.CrossRefGoogle Scholar
  87. ONE (2013). Evolution de la couverture de forêts naturelles à Madagascar (2005- 2010). Antananarivo: Office National pour l’Environnement. www.pnae.mg/index.php/Autres/evolution-de-la-couverture-de-forets-naturelles-a-madagascar-2005-2010.html. Accessed 26 Nov 2015.
  88. Palstra, F. P., & Fraser, D. J. (2012). Effective/census population size ratio estimation: a compendium and appraisal. Ecology and Evolution, 2(9), 2357–2365.PubMedPubMedCentralCrossRefGoogle Scholar
  89. Paradis, E., Claude, J., & Strimmer, K. (2004). APE: analyses of phylogenetics and evolution in R language. Bioinformatics, 20(2), 289–290.PubMedCrossRefGoogle Scholar
  90. Peakall, R. O. D., & Smouse, P. E. (2006). GENALEX 6: genetic analysis in excel. population genetic software for teaching and research. Molecular Ecology Notes, 6(1), 288–295.CrossRefGoogle Scholar
  91. Peery, M. Z., Kirby, R., Reid, B. N., Stoelting, R., Doucet-Bëer, E., Robinson, S., et al. (2012). Reliability of genetic bottleneck tests for detecting recent population declines. Molecular Ecology, 21(14), 3403–3418.PubMedCrossRefGoogle Scholar
  92. Pemberton, J. (2004). Measuring inbreeding depression in the wild: the old ways are the best. Trends in Ecology & Evolution, 19(12), 613–615.CrossRefGoogle Scholar
  93. Petit, R. J., Aguinagalde, I., de Beaulieu, J.-L., Bittkau, C., Brewer, S., Cheddadi, R., et al. (2003). Glacial refugia: hotspots but not melting pots of genetic diversity. Science, 300(5625), 1563–1565.PubMedCrossRefGoogle Scholar
  94. Pimm, S. L., & Brooks, T. (2013). Conservation: forest fragments, facts, and fallacies. Current Biology, 23(24), 1098–1101.CrossRefGoogle Scholar
  95. Pimm, S. L., & Raven, P. (2000). Biodiversity: extinction by numbers. Nature, 403(6772), 843–845.PubMedCrossRefGoogle Scholar
  96. Piry, S., Luikart, G., & Cornuet, J. M. (1999). Computer note. BOTTLENECK: A computer program for detecting recent reductions in the effective size using allele frequency data. Journal of Heredity, 90(4), 502.CrossRefGoogle Scholar
  97. Provan, J., & Bennett, K. D. (2008). Phylogeographic insights into cryptic glacial refugia. Trends in Ecology & Evolution, 23(10), 564–571.CrossRefGoogle Scholar
  98. Quéméré, E., Champeau, J., Besolo, A., Rasolondraibe, E., Rabarivola, C., Crouau-Roy, B., & Chikhi, L. (2010a). Spatial variation in density and total size estimates in fragmented primate populations: the golden-crowned sifaka (Propithecus tattersalli). American Journal of Primatology, 72(1), 72–80.PubMedCrossRefGoogle Scholar
  99. Quéméré, E., Crouau-Roy, B., Rabarivola, C., Louis, E. E., & Chikhi, L. (2010b). Landscape genetics of an endangered lemur (Propithecus tattersalli) within its entire fragmented range. Molecular Ecology, 19(8), 1606–1621.PubMedCrossRefGoogle Scholar
  100. Quéméré, E., Louis, E. E., Ribéron, A., Chikhi, L., & Crouau-Roy, B. (2010c). Non-invasive conservation genetics of the critically endangered golden-crowned sifaka (Propithecus tattersalli): high diversity and significant genetic differentiation over a small range. Conservation Genetics, 11(3), 675–687.CrossRefGoogle Scholar
  101. Quéméré, E., Amelot, X., Pierson, J., Crouau-Roy, B., & Chikhi, L. (2012). Genetic data suggest a natural prehuman origin of open habitats in northern Madagascar and question the deforestation narrative in this region. Proceedings of the National Academy of Sciences of the USA, 109(32), 13028–13033.PubMedPubMedCentralCrossRefGoogle Scholar
  102. R CoreTeam. (2014). R: A language and environment for statistical computing. http://www.R-project.org. Accessed 18 Nov 2014.
  103. Radespiel, U., Rakotondravony, R., & Chikhi, L. (2008). Natural and anthropogenic determinants of genetic structure in the largest remaining population of the endangered golden-brown mouse lemur, Microcebus ravelobensis. American Journal of Primatology, 70(9), 860–870.PubMedCrossRefGoogle Scholar
  104. Rakotoarisoa, G. (2010). Diversité génétique de Propithecus coquereli. PhD thesis, Univeristy of Antananarivo, Antananarivo.Google Scholar
  105. Rakotoarisoa, G., Shore, G., Mcguire, S., Engberg, S., Louis, E., & Brenneman, R. (2006). Characterization of 20 microsatellite marker loci in Coquerel’s sifaka (Propithecus coquereli). Molecular Ecology Notes, 6(4), 1119–1121.CrossRefGoogle Scholar
  106. Razafindrakoto, A., Andriantompohavana, R., Wohlhauser, S., Rajaobelina, S., Louis, E. E., Jr., & Brenneman, R. A. (2007). Forest fragment and range survey of the Ambararata-Maromokotra Loky River locale of northeastern Madagascar for golden-crowned sifaka (Propithecus tattersalli). Lemur News, 12, 29.Google Scholar
  107. Razakamaharavo, V. R., McGuire, S. M., Vasey, N., Louis, E. E., Jr., & Brenneman, R. A. (2010). Genetic architecture of two red ruffed lemur (Varecia rubra) populations of Masoala National Park. Primates, 51(1), 53–61.PubMedCrossRefGoogle Scholar
  108. Richard, A. F., Rakotomanga, P., & Schwartz, M. (1993). Dispersal by Propithecus verreauxi at Beza Mahafaly, Madagascar 1984–1991. American Journal of Primatology, 30(1), 1–20.CrossRefGoogle Scholar
  109. Roelke, M. E., Martenson, J. S., & O’Brien, S. J. (1993). The consequences of demographic reduction and genetic depletion in the endangered Florida panther. Current Biology, 3(6), 340–350.PubMedCrossRefGoogle Scholar
  110. Rousset, F. C. (2008). Genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Molecular Ecology Resources, 8(1), 103–106.PubMedCrossRefGoogle Scholar
  111. Salmona, J. (2014). Conservation, distribution and population size update of endangered nocturnal lemur species from Northern Madagascar, Rufford Small Grant final report. Rufford Small Grant Final Report No. 1 (p. 21). https://www.researchgate.net/profile/Jordi_Salmona/publication/262334029_Conservation_distribution_and_population_size_update_of_endangered_nocturnal_lemur_species_from_Northern_Madagascar_Rufford_Small_Grant_final_report/links/0c9605374f966d7a1a000000.pdf. Accessed 26 Nov 2015.
  112. Salmona, J. (2015). Comparative conservation genetics of several threatened lemur species living in fragmented environments. A glimpse through natural history of northern Madagascar lemurs. Ph.D Thesis (p. 330), Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa, Instituto Gulbenkian de Ciência, Oeiras Portugal.Google Scholar
  113. Salmona, J., Salamolard, M., Fouillot, D., Ghestemme, T., Larose, J., Centon, J.-F., et al. (2012). Signature of a pre-human population decline in the critically endangered Reunion Island endemic forest bird Coracina newtoni. PLoS ONE, 7(8), e43524.PubMedPubMedCentralCrossRefGoogle Scholar
  114. Salmona, J., Jan, F., Rasolondraibe, E., Zaranaina, R., Saïd Ousseni, D., Mohamed-Thani, I., et al. (2013a). Survey of the critically endangered Perrier’s sifaka (Propithecus perrieri) across most if its distribution range. Lemur News, 17, 9–12.Google Scholar
  115. Salmona, J., Zaonarivelo, J. R., & Banks, M. A. (2013b). Analamerana and Andrafiamena, site-based action plan for Perrier’s sifaka conservation. In C. Schwitzer, R. A. Mittermeier, N. Davies, S. E. Johnson, J. Ratsimbazafy, J. Razafindramanana, et al. (Eds.), Lemurs of Madagascar: A strategy for their conservation 2013–2016 (pp. 140–141). Bristol, UK: IUCN SSC Primate Specialist Group, Bristol Conservation and Science Foundation, and Conservation International.Google Scholar
  116. Salmona, J., Rasolondraibe, E., Jan, F., Besolo, A., Rakotoarisoa, H., Meyler, S. V., et al. (2014). Conservation status and abundance of the crowned sifaka (Propithecus coronatus). Primate Conservation, 28, 73–83.CrossRefGoogle Scholar
  117. Schwitzer, C., Arnoult, O., & Rakotosamimanana, B. (2006). An international conservation and research programme for Perrier’s sifaka (Propithecus perrieri Lavauden, 1931) in northern Madagascar. Lemur News, 11, 13.Google Scholar
  118. Schwitzer, C., Mittermeier, R. A., Davies, N., Johnson, S., Ratsimbazafy, J., Razafindramanana, J., et al. (2013). Lemurs of Madagascar: A strategy for their conservation 2013–2016 (p. 185). Bristol, UK: IUCN SSC Primate Specialist Group, Bristol Conservation and Science Foundation, and Conservation International.Google Scholar
  119. Schwitzer, C., Chikhi, L., Donati, G., Irwin, M., Johnson, S. E., Mittermeier, R. A., et al. (2014a). Protecting lemurs–response. Science (New York), 344(6182), 358.CrossRefGoogle Scholar
  120. Schwitzer, C., Mittermeier, R., Johnson, S., Donati, G., Irwin, M., Peacock, H., et al. (2014b). Averting lemur extinctions amid Madagascar’s political crisis. Science, 343(6173), 842–843.PubMedCrossRefGoogle Scholar
  121. Soulé, M. E. (1980). Thresholds for survival: maintaining fitness and evolutionary potential. Conservation Biology, 111, 124.Google Scholar
  122. Storz, J. F., & Beaumont, M. A. (2002). Testing for genetic evidence of population expansion and contraction: an empirical analysis of microsatellite DNA variation using a hierarchical Bayesian model. Evolution, 56(1), 154–166.PubMedCrossRefGoogle Scholar
  123. Tajima, F. (1989). The effect of change in population size on DNA polymorphism. Genetics, 123(3), 597.PubMedPubMedCentralGoogle Scholar
  124. Tulloch, A. I. T., Barnes, M. D., Ringma, J., Fuller, R. A., & Watson, J. E. M. (2015). Understanding the importance of small patches of habitat for conservation. Journal of Applied Ecology. doi: 10.1111/1365-2664.12547.Google Scholar
  125. Vallet, D., Petit, E. J., Gatti, S., Levréro, F., & Ménard, N. (2008). A new 2CTAB/PCI method improves DNA amplification success from faeces of Mediterranean (Barbary macaques) and tropical (lowland gorillas) primates. Conservation Genetics, 9(3), 677–680.CrossRefGoogle Scholar
  126. van Oosterhout, C., Hutchinson, W. F., Wills, D. P., & Shipley, P. (2004). MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes, 4(3), 535–538.CrossRefGoogle Scholar
  127. Vasey, N. (1997). How many red ruffed lemurs are left? International Journal of Primatology, 18(2), 207–216.CrossRefGoogle Scholar
  128. Vieilledent, G., Grinand, C., & Vaudry, R. (2013). Forecasting deforestation and carbon emissions in tropical developing countries facing demographic expansion: a case study in Madagascar. Ecology and Evolution, 3(6), 1702–1716.PubMedPubMedCentralCrossRefGoogle Scholar
  129. Walker, F. M., Sunnucks, P., & Taylor, A. C. (2008). Evidence for habitat fragmentation altering within-population processes in wombats. Molecular Ecology, 17(7), 1674–1684.PubMedCrossRefGoogle Scholar
  130. Waples, R. S., & Do, C. H. I. (2008). LDNE: a program for estimating effective population size from data on linkage disequilibrium. Molecular Ecology Resources, 8(4), 753–756.PubMedCrossRefGoogle Scholar
  131. Weir, B. S., & Cockerham, C. C. (1984). Estimating F-statistics for the analysis of population structure. Evolution, 38(6), 1358–1370.CrossRefGoogle Scholar
  132. Wittke-Thompson, J. K., Pluzhnikov, A., & Cox, N. J. (2005). Rational inferences about departures from Hardy-Weinberg equilibrium. The American Journal of Human Genetics, 76(6), 967–986.PubMedCrossRefGoogle Scholar
  133. Wootton, J. T., & Pfister, C. A. (2013). Experimental separation of genetic and demographic factors on extinction risk in wild populations. Ecology, 94(10), 2117–2123.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Jordi Salmona
    • 1
    Email author
  • Helena Teixeira
    • 1
  • Emmanuel Rasolondraibe
    • 2
  • Isa Aleixo-Pais
    • 1
  • Célia Kun-Rodrigues
    • 1
  • Ando Nantenaina Rakotonanahary
    • 2
  • Fabien Jan
    • 1
  • Clément Joseph Rabarivola
    • 2
  • John Rigobert Zaonarivelo
    • 3
  • Nicole Volasoa Andriaholinirina
    • 2
  • Lounès Chikhi
    • 1
    • 4
    • 5
    Email author
  1. 1.Instituto Gulbenkian de CiêncaOeirasPortugal
  2. 2.Département de Biologie Animale et EcologieFaculté des Sciences, de Technologies et de l’Environnement de MahajangaMahajangaMadagascar
  3. 3.Département des Sciences de la Nature et de l’EnvironnementUniversité d’AntsirananaAntsirananaMadagascar
  4. 4.Laboratoire Evolution & Diversité BiologiqueUMR 5174 CNRS – Université Paul SabatierToulouseFrance
  5. 5.Université de Toulouse, UMR 5174 EDBToulouseFrance

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