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Population genetics and abundance of the Endangered grey-headed lemur Eulemur cinereiceps in south-east Madagascar: assessing risks for fragmented and continuous populations

  • Rick A. Brenneman (a1), Steig E. Johnson (a2), Carolyn A. Bailey (a1), Christina Ingraldi (a2), Kira E. Delmore (a2), Tracy M. Wyman (a2), Hubert E. Andriamaharoa (a3), Fidimalala B. Ralainasolo (a4), Jonah H. Ratsimbazafy (a4) and Edward E. Louis (a1)...
Abstract

Knowledge of both population size and genetic diversity is critical for assessing extinction risk but few studies include concurrent estimates of these two components of population biology. We conducted an investigation of population density and size, and genetic variation and past demographic events, of the Endangered grey-headed lemur Eulemur cinereiceps in south-east Madagascar. We estimated lemur density using line-transect surveys and used satellite imagery to calculate forest fragment area in three localities. We collected tissue samples from 53 individuals and used 26 polymorphic microsatellite loci to obtain measures of population structure (divergence and diversity) across these localities. We tested the probability of past bottleneck events using three models. Contrary to expectation, there were no significant differences in population density across localities. Genetic diversity decreased, but not significantly, with decreasing habitat area and population size. We found a higher likelihood of past bottleneck events in the fragmented coastal populations. The low population size and prior decline in diversity in coastal patches are consistent with their isolation, anthropogenic disturbance, and exposure to cyclone activity. The similarities in the estimates of density between continuous and fragmented sites may indicate recent population growth in the fragments but these populations nevertheless remain at risk from reduced levels of genetic variation. These patterns should be confirmed with more extensive sampling across the limited range of E. cinereiceps.

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      Population genetics and abundance of the Endangered grey-headed lemur Eulemur cinereiceps in south-east Madagascar: assessing risks for fragmented and continuous populations
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      Population genetics and abundance of the Endangered grey-headed lemur Eulemur cinereiceps in south-east Madagascar: assessing risks for fragmented and continuous populations
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      Population genetics and abundance of the Endangered grey-headed lemur Eulemur cinereiceps in south-east Madagascar: assessing risks for fragmented and continuous populations
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Corresponding author
*Grewcock Center for Conservation and Research, Omaha’s Henry Doorly Zoo, 3701 South 10th St, Omaha, Nebraska 68107, USA. E-mail rabr@omahazoo.com
References
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Andriantompohavana, R., Morelli, T.L., Behncke, S.M., Engberg, S.E., Brenneman, R.A. & Louis, E.E. (2007) Characterization of twenty Eulemur-specific microsatellite loci characterized in two populations of the red-bellied brown lemur, Eulemur rubriventer. Molecular Ecology Notes, 7, 11621165.
Bazin, E., Glémin, S. & Galtier, N. (2006) Population size does not influence mitochondrial genetic diversity in animals. Science, 312, 570572.
Bergl, R.A., Bradley, B.J., Nsubuga, A. & Vigilant, L. (2008) Effects of habitat fragmentation, population size and demographic history on genetic diversity: the Cross River gorilla in comparative context. American Journal of Primatology, 70, 848859.
Burney, D.A. (1999) Rates, patterns, and processes of landscape transformations and extinction in Madagascar. In Extinctions in Near Time: Causes, Contexts, and Consequences (eds MacPhee, R.D.E. & Sues, H.D.), pp. 145164. Kluwer Academic/Plenum Publishers, New York, USA.
Caballero, A. (1994) Development in the prediction of effective population size. Heredity, 73, 657679.
Caughley, G. (1994) Directions in conservation biology. Journal of Animal Ecology, 63, 215244.
Chiarello, A.G. (2000) Density and population size of mammals in remnants of Brazilian Atlantic Forest. Conservation Biology, 14, 16491657.
Cornuet, J.M. & Luikart, G. (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics, 144, 20012014.
Dewar, R.E. & Richard, A.F. (2007) Evolution in the hypervariable environment of Madagascar. Proceedings of the National Academy of Sciences of the United States of America, 104, 1372313727.
DiBatista, J.D. (2008) Patterns of genetic variation in anthropogenically impacted populations. Conservation Genetics, 9, 141156.
Dieringer, D. & Schlötterer, C. (2003) Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Molecular Ecology Notes, 3, 167169.
Di Rienzo, A., Peterson, A.C., Garza, J.C., Valdes, A.M., Slatkin, M. & Freimer, N.B. (1994) Mutational processes of simple-sequence repeat loci in human populations. Proceedings of the National Academy of Sciences of the United States of America, 91, 31663170.
Estrada, A. & Coates-Estrada, R. (1996) Tropical rain forest fragmentation and wild populations of primates at Los Tuxtlas, Mexico. International Journal of Primatology, 17, 759783.
Ezard, T.H.G. & Travis, J.M.J. (2006) The impact of habitat loss and fragmentation on genetic drift and fixation time. OIKOS, 114, 367375.
GLCF (2010) Global Land Cover Facility. Http://glcf.umiacs.umd.edu [accessed 27 October 2008].
Godfrey, L.R. & Irwin, M.T. (2007) The evolution of extinction risk: past and present anthropogenic impacts on the primate communities of Madagascar. Folia Primatologica, 78, 405419.
Goosens, B., Chikhi, L., Jalil, M.F., Ancrenaz, M., Lackman-Ancrenaz, I., Mohamed, M. et al. . (2005) Patterns of genetic diversity and migration in increasingly fragmented and declining orang-utan (Pongo pygmaeus) populations from Sabah, Malaysia. Molecular Ecology, 15, 441456.
Goudet, J. (2002) FSTAT, a Program to Estimate and Test Gene Diversities and Fixation Indices (Version 2.9.3). Http://www2.unil.ch/popgen/softwares/fstat.htm [accessed 23 July 2009].
Gravitol, A.D., Ballou, J.D. & Fleischer, R.C. (2001) Microsatellite variation within and among recently fragmented populations of the golden lion tamarin (Leontopithecus rosalia). Conservation Genetics, 2, 19.
Guo, S.W. & Thompson, E.A. (1992) Performing the exact test of Hardy–Weinberg proportion for multiple alleles. Biometrics, 48, 361372.
Hardy, O.J. & Vekemans, X. (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Molecular Ecology Notes, 2, 618620.
Hedrick, P.W. (2005) Genetics of Populations. Jones & Bartlett Publishers, Sudbury, USA.
Hill, W.G. (1981) Estimation of linkage disequilibrium in randomly mating populations. Heredity, 33, 229239.
Irwin, M.T. (2008) Diademed sifaka (Propithecus diadema) ranging and habitat use in continuous and fragmented forest: higher density but lower viability in fragments? Biotropica, 40, 231240.
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, 204218.
IUCN (2009) The IUCN Red List of Threatened Species. Http://www.iucnredlist.org [accessed 28 September 2009].
Jekielek, J. & Strobeck, C. (1999) Characterization of polymorphic brown lemur (Eulemur fulvus) microsatellite loci and their amplification in the family Lemuridae. Molecular Ecology, 8, 901903.
Johnson, S.E. (2002) Ecology and speciation in brown lemurs: white-collared lemurs (Eulemur albocollaris) and hybrids (Eulemur albocollaris X Eulemur fulvus rufus) in south-eastern Madagascar. PhD dissertation, University of Texas, Austin, USA.
Johnson, S.E., Ingraldi, C., Ralainasolo, F.R., Andriamaharoa, H.E., Ludovic, R., Birkinshaw, C.R. et al. . (2011) Gray-headed lemur (Eulemur cinereiceps) abundance and forest structure dynamics at Manombo, Madagascar. Biotropica, 43, 371379.
Johnson, S.E. & Overdorff, D.J. (1999) A census of brown lemurs (Eulemur fulvus sspp.) in south-eastern Madagascar: methods-testing and conservation implications. American Journal of Primatology, 47, 5160.
Kalinowski, S.T. & Waples, R.S. (2002) Relationship of effective to census size in fluctuating populations. Conservation Biology, 16, 129136.
Kanthaswamy, S. & Smith, D.G. (2002) Population subdivision and gene flow among wild orangutans. Primates, 43, 315327.
Kawamoto, Y., Tomari, K.I., Kawai, S. & Kawamoto, S. (2008) Genetics of the Shimokita macaque populations suggest an ancient bottleneck. Primates, 49, 3240.
Lande, R. (1988) Genetics and demography in biological conservation. Science, 241, 14551460.
Lande, R. (1995) Mutation and conservation. Conservation Biology, 9, 782791.
Lehman, S.M., Rajaonson, A. & Day, S. (2006a) Edge effects and their influence on lemur density and distribution in south-east Madagascar. American Journal of Physical Anthropology, 129, 232241.
Lehman, S.M., Ratsimbazafy, J., Rajaonson, A. & Day, S. (2006b) Decline of Propithecus diadema edwardsi and Varecia variegata variegata (Primates: Lemuridae) in south-east Madagascar. Oryx, 40, 108111.
Lowry, P.P., Schatz, G.E. & Phillipson, P.B. (1997) The classification of natural and anthropogenic vegetation in Madagascar. In Natural Change and Human Impact in Madagascar (eds Goodman, S.M. & Patterson, B.D.), Smithsonian Institution Scholarly Press, Washington, DC, USA.
Luikart, G. & Cornuet, J.-M. (1998) Empirical evaluation of a test for detecting recent historical population bottlenecks. Conservation Biology, 12, 228237.
Mills, S.M. & Smouse, P.E. (1994) Demographic consequences of inbreeding in remnant populations. American Naturalist, 144, 412431.
Mittermeier, R.A., Konstant, W.R., Hawkins, F., Louis, E.E., Langrand, O., Ratsimbazafy, J. et al. . (2006) Lemurs of Madagascar. Conservation International, Washington, DC, USA.
Mittermeier, R.A., Ratsimbazafy, J., Rylands, A.B., Williamson, L., Oates, J.F., Mbora, D. et al. . (2007) Primates in peril: the world’s 25 most endangered primates, 2006–2008. Primate Conservation, 22, 140.
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, 12571271.
Overdorff, D.J., Merenlender, A.M., Talata, P., Telo, A. & Forward, Z.A. (1999) Life history of Eulemur fulvus rufus from 1988–1998 in south-eastern Madagascar. American Journal of Physical Anthropology, 108, 295310.
Peel, D., Ovenden, J.R. & Peel, S.L. (2004) NeEstimator: Software for Estimating Effective Population Size, Version 1.3. Department of Primary Industries and Fisheries, Queensland Government, City East, Queensland, Australia.
Piry, S., Luikart, G. & Cornuet, J.M. (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. Journal of Heredity, 90, 502503.
Pudovkin, A.I., Zaykin, D.V. & Hedgecock, D. (1996) On the potential for estimating the effective number of breeders from heterozygote-excess progeny. Genetics, 144, 383387.
Queller, D.C. & Goodnight, K.F. (1989) Estimating relatedness using genetic markers. Evolution, 43, 258275.
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, 860870.
Ratsimbazafy, J.H. (2002) On the brink of extinction and the process of recovery: responses of black-and-white ruffed lemurs (Varecia variegata variegata) to disturbance in Manombo Forest, Madagascar. PhD Dissertation, State University of New York, Stony Brook, USA.
Ratsimbazafy, J.H., Ramarosandratana, H.V. & Zaonarivelo, R.J. (2002) How do black-and-white ruffed lemurs still survive in a highly disturbed habitat? Lemur News, 7, 710.
Raymond, M. & Rousset, F. (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity, 86, 248249.
Razakamaharavo, V., McGuire, S.M., Louis, E.E. & Brenneman, R.A. (2009) Genetic architecture of regional red ruffed lemur (Varecia rubra) populations in Masoala National Park of Madagascar. Primates, 51, 5361.
Sambrook, J., Fritch, E.F. & Maniatus, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, New York, USA.
Slate, J., Marshall, T.C. & Pemberton, J.M. (2000) A retrospective assessment of the accuracy of the paternity inference program CERVUS. Molecular Ecology, 9, 801808.
Slatkin, M. (1985) Gene flow in natural populations. Annual Review of Ecology and Systematics, 16, 393430.
Tokiniaina, H., Bailey, C.A., Shore, G.M., Delmore, K.E., Johnson, S.E., Louis, E.E. & Brenneman, R.A. (2009) Characterization of 18 microsatellite marker loci in the white-collared lemur (Eulemur cinereiceps). Conservation Genetics, 10, 14591462.
Van Oosterhaut, C., Hutchinson, W.F., Wills, D.P.M. & Shipley, P. (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes, 4, 535538.
Waples, R.S. (1991) Genetic methods for estimating the effective size of cetacean populations. In Genetic Ecology of Whales and Dolphins, Special Issue 13 (ed. Hoelzel, A.R.), pp. 279300. International Whaling Commission, London, UK.
Warren, B.H., Strasberg, D., Bruggemann, J.H., Prys-Jones, R.P. & Thébaud, C. (2010) Why does the biota of the Madagascar region have such a strong Asiatic flavour? Cladistics, 26, 526538.
Weir, B. & Cockerham, C.C. (1984) Estimating F-statistics for the analysis of population structure. Evolution, 38, 13581370.
Whitesides, G., Oates, J., Green, S. & Kluberdanz, R. (1988) Estimating primate densities from transects in a West African rain forest: a comparison of techniques. Journal of Animal Ecology, 57, 345367.
Whitlock, M.C. (2000) Fixation of new alleles and the extinction of small populations: drift load, beneficial alleles, and sexual selection. Evolution, 54, 18551861.
Yoder, A.D. & Nowack, M.D. (2006) Has vicariance or dispersal been the predominant biogeographic force in Madagascar? Only time will tell. Annual Review of Ecology, Evolution, and Systematics, 37, 405431.
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