Population Ecology

, Volume 53, Issue 1, pp 229–240 | Cite as

Historical demography of a wild lemur population (Propithecus verreauxi) in southwest Madagascar

Original Article


The human colonization of Madagascar is associated with the extinction of numerous lemur species. However, the degree to which humans have negatively influenced the historical population dynamics of extant lemur species is not well understood. This study employs genetic and demographic analyses to estimate demographic parameters relating to the historical population dynamics of a wild lemur population, Verreaux’s sifaka (Propithecus verreauxi). The genetic analyses are used to determine whether this population experienced a historically recent (i.e., within the last 2000 years) population bottleneck, as well as to estimate the historical population growth rate and the timing of any changes in population size in the past. In addition, a retrospective demographic analysis is used to determine sources of variation and covariation in the sifaka life cycle and how variation in life-cycle transitions contributes to variation in population growth rate. The genetic analyses indicate that the sifaka population did not experience a recent population bottleneck; however, the historical population growth rate was negative, indicating that the ancestral population size was much larger than the current size. The timing of the ancestral population decline has a point estimate of 2300 years ago, but with large credible intervals: 3611–1736 years ago. This point estimate corresponds with the first evidence for human arrival to Madagascar. Climatic variation has also likely influenced past (and current) population dynamics due to stochastic annual rainfall patterns and climatic desiccation, the latter of which began in southwestern Madagascar around 4000 years ago. Variation in the survival of 2-year-old animals as well as large adult females makes the largest contribution to variation in population growth rate. In the absence of more explicit models pertaining to historical population dynamics, it is difficult to attribute the negative population growth rate of this species solely to a single factor (e.g., hunting, habitat destruction).


Habitat disturbance Hunting Life-table response experiment Population growth rate Sifaka 



I am grateful to the government of Madagascar and the ANGAP authorities for permission to conduct this study. Various friends and colleagues contributed to data collection analyzed in this paper, and I am very grateful for the friendship and help. These individuals include Joel Ratsirarson, Alison Richard, Marion Schwartz, Robert Dewar, Diane Brockman, Kashka Kubzdela, Enafa, Elahavelo, Emady Rigobert, and Ellis Edidy. In addition to the aforementioned individuals, I am also very grateful for the friendship and support provided by Ibrahim Antho Youssouf Jacky, Jeannin Ranaivonasy, and Roshna Wunderlich in the field. I thank Hal Caswell and other members of the mathematical ecology group at Woods Hole Oceanographic Institution for their help in teaching me some of the analyses used in this paper; any errors are mine, however, not theirs. Moxie continues to teach me about issues in animal conservation. Many thanks to the editor at Population Ecology and especially to three anonymous reviewers who thoughtfully critiqued this manuscript and made the resulting publication much clearer and more responsible. This research was supported by National Science Foundation Postdoctoral Fellowship in Biological Informatics (DBI 0305074) and a National Science Foundation Research Starter grant (DEB 0531988) and a National Science Foundation Full proposal (BCS 0960417). All necessary permits (CITES, IACUC, and Biohazard) were obtained and approved prior to conducting this research. Support for the Beza Mahafaly Monitoring Team is kindly provided by the Liz Claiborne and Art Ortenberg Foundation.


  1. Alroy J (2001) A multispecies overkill simulation of the end-Pleistocene megafaunal mass extinction. Science 292:1893–1896CrossRefPubMedGoogle Scholar
  2. Aspi J, Roininen E, Ruokonen M, Kojola I, Vila C (2006) Genetic diversity, population structure, effective population size and demographic history of the Finnish wolf population. Mol Ecol 15:1561–1576CrossRefPubMedGoogle Scholar
  3. Beaumont MA (1999) Detecting population expansion or decline using microsatellites. Genetics 153:2013–2029PubMedGoogle Scholar
  4. Brault S, Caswell H (1993) Podspecifc demography of killer whales (Orcinus orca). Ecology 74:1444–1454CrossRefGoogle Scholar
  5. Brockman D (1999) Reproductive behavior of female Propithecus verreauxi at Beza Mahafaly, Madagascar. Int J Primatol 20:375–398CrossRefGoogle Scholar
  6. Brockman DK, Dollar LJ, Godfrey LR (2008) Evidence of wildcat (Felis silvestris) predation on Propithecus verreauxi at Beza Mahafaly, Madagascar. Int J Primatol 29:135–152CrossRefGoogle Scholar
  7. Burney DA (1993) Late Holocene environmental changes in arid southwestern Madagascar. Quat Res 40:98–106CrossRefGoogle Scholar
  8. Burney DA (1999) Rates, patterns, and the processes of landscape transformation and extinction in Madagascar. In: MacPhee RDE (ed) Extinctions in near time: causes, contexts, and consequences. Plenum Press, New York, pp 145–164Google Scholar
  9. Burney DA, Flannery TF (2006) Response to Wroe et al.: island extinctions versus continental extinctions. Trends Ecol Evol 21:63–64CrossRefGoogle Scholar
  10. Burney DA, Burney LP, Godfrey LR, Jungers WL, Goodman SM, Wright HT, Jull AJT (2004) A chronology for late prehistoric Madagascar. J Hum Evol 47:25–63CrossRefPubMedGoogle Scholar
  11. Busch JD, Waser PM, DeWoody A (2007) Recent demographic bottlenecks are not accompanied by a genetic signature in banner-tailed kangaroo rats (Dipodomys spectabilis). Mol Ecol 16:2450–2462CrossRefPubMedGoogle Scholar
  12. Caswell H (1982) Life history theory and the equilibrium status of populations. Am Nat 120:317–339CrossRefGoogle Scholar
  13. Caswell H (1996) Analysis of life table response experiments II. Alternative parameterizations for size- and stage-structured models. Ecol Model 88:73–82CrossRefGoogle Scholar
  14. Caswell H (2000) Prospective and retrospective perturbation analyses: their roles in conservation biology. Ecology 81:619–627CrossRefGoogle Scholar
  15. Caswell H (2001) Matrix population models. Sinauer Press, SunderlandGoogle Scholar
  16. Charlesworth B (1994) Evolution in age-structured populations. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  17. Cincotta RP, Wisnewski J, Engelman R (2000) Human population and biodiversity hotspots. Nature 404:990–992CrossRefPubMedGoogle Scholar
  18. Coale AJ (1972) The growth and structure of human populations: a mathematical approach. Princeton University Press, PrincetonGoogle Scholar
  19. Dewar RE (2003) Relation between human ecological pressure and the vertebrate extinctions. In: Goodman SM, Benstead JP (eds) The natural history of Madagascar. University of Chicago Press, Chicago, pp 119–122Google Scholar
  20. Dewar RE, Richard AF (2007) Evolution in the hypervariable environment of Madagascar. Proc Natl Acad Sci USA 104:13723–13727CrossRefPubMedGoogle Scholar
  21. Dewar RE, Wallis JR (1999) Geographical patterning of interannual rainfall variability in the tropics and near tropics: an L-moments approach. J Climate 12:3457–3466CrossRefGoogle Scholar
  22. Dewar RE, Wright HT (1993) The culture history of Madagascar. J World Prehist 7:417–466CrossRefGoogle Scholar
  23. Di Rienzo A, Peterson AC, Garza JC, Valdes AM, Slatkin M, Freimer NB (1994) Mutational processes of simple sequence repeat loci in human populations. Proc Natl Acad Sci USA 91:3166–3170CrossRefPubMedGoogle Scholar
  24. Diamond JM (1989) The past, present, and future of human-caused extinctions. Philos Trans Roc Soc Lond B 325:469–477CrossRefGoogle Scholar
  25. Duncan RP, Blackburn TM, Worthy TH (2002) Prehistoric bird extinctions and human hunting. Proc Roy Sci B 269:517–521CrossRefGoogle Scholar
  26. Fiedel S, Haynes G (2004) A premature burial: comments on Grayson and Meltzer’s “Requiem for overkill”. J Arch Sci 31:121–131CrossRefGoogle Scholar
  27. Fujiwara M, Caswell H (2002) Estimating population projection matrices from multi-stage mark-recapture data. Ecology 83:3257–3265Google Scholar
  28. Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318CrossRefPubMedGoogle Scholar
  29. Godfrey LR, Irwin MT (2007) The evolution of extinction risk: past and present anthropogenic impacts on the primate communities of Madagascar. Folia Primatol 78:405–419CrossRefPubMedGoogle Scholar
  30. Godfrey LR, Jungers WL (2002) Quaternary fossil lemurs. In: Hartwig WC (ed) The primate fossil record. Cambridge University Press, Cambridge, pp 97–122Google Scholar
  31. Godfrey LR, Jungers WL, Schwartz GT (2006) Ecology and extinction of Madagascar’s subfossil lemurs. In: Gould L, Sauther ML (eds) Lemurs: ecology and adaptation. Springer, Berlin, pp 41–64Google Scholar
  32. Goodman SM, Benstead JP (eds) (2003) The natural history of Madagascar. University of Chicago Press, ChicagoGoogle Scholar
  33. Goodman SM, Patterson BD (eds) (1997) Natural change and human impact in Madagascar. Smithsonian Institution Press, Washington, DCGoogle Scholar
  34. Grayson DK, Meltzer DJ (2003) A requiem for North American overkill. J Arch Sci 30:585–593CrossRefGoogle Scholar
  35. Grayson DK, Meltzer DJ (2004) North American overkill continued? J Arch Sci 31:133–136CrossRefGoogle Scholar
  36. Guthrie RD (2006) New carbon dates link climatic change with human colonization and Pleistocene extinctions. Nature 441:207–209CrossRefPubMedGoogle Scholar
  37. Hailer F, Helander B, Folkestad AO, Ganusevich SA, Garstad S, Hauff P, Koren C, Nygard T, Volke V, Vila C, Ellegren H (2006) Bottlenecked but long-lived: high genetic diversity retained in white-tailed eagles upon recovery from population decline. Biol Lett 2:316–319CrossRefPubMedGoogle Scholar
  38. Holdaway RN, Jacomb C (2000) Rapid extinction of the moas (Aves: Dinornithiformes): Model, test, and implications. Science 287:2250–2254CrossRefPubMedGoogle Scholar
  39. Jones JPG, Andriamarovololona MM, Hockley N (2008) The importance of taboos and social norms to conservation in Madagascar. Conserv Biol 22:976–986CrossRefPubMedGoogle Scholar
  40. Kaufmann JC, Tsirahamba S (2006) Forests and thorns: conditions of change affecting Mahafale pastoralists in southwestern Madagascar. Conserv Soc 4:231–261Google Scholar
  41. Kull CA (2003) Fire and the management of highland vegetation. In: Goodman SM, Benstead JP (eds) The natural history of Madagascar. University of Chicago Press, Chicago, pp 153–157Google Scholar
  42. Kuo CH, Janzen FJ (2004) Genetic effects of a persistent bottleneck on a natural population of ornate box turtles (Terrapene ornata). Conserv Genet 5:425–437CrossRefGoogle Scholar
  43. Lande R (1982) A quantitative genetic theory of life history evolution. Ecology 63:607–615CrossRefGoogle Scholar
  44. Lawler RR (2007) Fitness and extra-group reproduction in male Verreaux’s sifaka (Propithecus verreauxi verreauxi). Am J Phys Anthropol 132:267–277CrossRefPubMedGoogle Scholar
  45. Lawler RR (2008) Testing for a historical population bottleneck in wild Verreaux’s sifaka (Propithecus verreauxi verreauxi) using microsatellite data. Am J Primatol 70:990–994CrossRefPubMedGoogle Scholar
  46. Lawler RR (2010) Genetic parentage data an effective population size: Examples from Verrreaux’s sifaka. In: DiFiore A, Harrison T (eds) Molecular primatology. Cambridge University Press, Cambridge (in press)Google Scholar
  47. Lawler RR, Richard AF, Riley MA (2001) Characterization and screening of microsatellite loci in a wild lemur population (Propithecus verreauxi verreauxi). Am J Primatol 55:253–259CrossRefPubMedGoogle Scholar
  48. Lawler RR, Richard AF, Riley MA (2003) Genetic population structure of the white sifaka (Propithecus verreauxi verreauxi) at Beza Mahafaly Special Reserve, southwest Madagascar (1992–2001). Mol Ecol 12:2301–2317CrossRefGoogle Scholar
  49. Lawler RR, Richard AF, Dewar RE, Schwartz M, Ratsirarson J, Caswell H (2009) Demography of a wild lemur population in a stochastic rainfall environment. Oecologia 161:491–504CrossRefPubMedGoogle Scholar
  50. Lingard MN, Raharison E, Rabakonandrianina T, Rakotoarisoa A, Elmqvist T (2003) The role of local taboos in conservation and management of species: the radiated tortoise in Southern Madagascar. Conserv Soc 1:223–246Google Scholar
  51. Loudon JE, Sauther ML, Fish KD, Hunter-Ishikawa M, Youssouf JI (2006) One reserve, three primates: applying a holistic approach to understand the interconnections among ring-tailed lemurs (Lemur catta), Verreaux’s sifaka (Propithecus verreauxi), and humans (Homo sapiens) at Beza Mahafaly Special Reserve, Madagascar. Ecol Env Anthropol 2:54–74Google Scholar
  52. Lucchini V, Galov A, Randi E (2004) Evidence of genetic distinction and long-term population decline in wolves (Canis lupus) in the Italian Apennines. Mol Ecol 13:523–536CrossRefPubMedGoogle Scholar
  53. Markolf M, Roos C, Kappeler P (2008) Genetic and demographic consequences of a rapid reduction in population size in a solitary lemur (Mirza coquereli). Open Conserv Biol J 2:21–29CrossRefGoogle Scholar
  54. Martin PS (1973) The discovery of America. Science 179:969–974CrossRefPubMedGoogle Scholar
  55. Miller GH, Magee JW, Johnson BJ, Fogel ML, Spooner NA, McCulloch MT, Ayliffe LK (1999) Pleistocene extinction of Genyornis newtoni: human impact on Australian Megafauna. Science 283:205–208CrossRefPubMedGoogle Scholar
  56. Mittermeier RA, Konstant WR, Hawkins F, Louis EE, Langrand O, Ratsimbazafy J, Rasoloarison R, Ganzhorn JU, Rajaobelina S, Tattersall I, Meyer DM (2006) Lemurs of Madagascar. Conservation International (Tropical Field Guide Series), Washington, DCGoogle Scholar
  57. Nielsen R, Beaumont RA (2009) Statistical inference in phylogeography. Mol Ecol 18:1034–1047CrossRefPubMedGoogle Scholar
  58. Nunney L (1993) The influence of mating system and overlapping generations on effective population size. Evolution 47:1329–1341CrossRefGoogle Scholar
  59. 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
  60. Olson SH (1984) The robe of the ancestors: forests in the history of Madagascar. J Forest Hist 28:174–186CrossRefGoogle Scholar
  61. Paulay G (1994) Biodiversity on oceanic islands: its origin and extinction. Am Zool 34:134–144Google Scholar
  62. Perez VR, Godfrey LR, Nowak-Kemp M, Burney DA, Ratsimbazafy J, Vasey N (2005) Evidence of butchery of giant lemurs in Madagascar. J Hum Evol 49:722–742CrossRefPubMedGoogle Scholar
  63. Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503CrossRefGoogle Scholar
  64. Razakamaharavo V, McGuire SM, Vasey N, Louis EE Jr, Brenneman RA (2009) Genetic architecture of two red ruffed lemur (Varecia rubra) populations of Masoala National Park. Primates 51:53–61CrossRefPubMedGoogle Scholar
  65. Richard AF, Dewar RE (1990) Lemur ecology. Annu Rev Ecol Syst 22:145–175CrossRefGoogle Scholar
  66. Richard AF, Rakotomanga P, Schwartz M (1993) Dispersal by Propithecus verreauxi at Beza Mahafaly, Madagascar. Am J Primatol 30:1–20CrossRefGoogle Scholar
  67. Richard AF, Dewar RE, Schwartz M, Ratsirarson J (2000) Mass change, environmental variability and female fertility in wild Propithecus verreauxi. J Hum Evol 39:381–391CrossRefPubMedGoogle Scholar
  68. Richard AF, Dewar RE, Schwartz M, Ratsirarson J (2002) Life in the slow lane? Demography and life histories of male and female sifaka (Propithecus verreauxi verreauxi). J Zool Lond 256:421–436CrossRefGoogle Scholar
  69. Roberts RG, Flannery TF, Ayliffe LK, Yoshida H, Olley JM, Prideaux GJ, Laslett GM, Baynes A, Smith MA, Jones R, Smith BL (2001) New ages for the last Australian megafauna: continent-wide extinction about 46,000 years ago. Science 292:1888–1892CrossRefPubMedGoogle Scholar
  70. Roff DA (1997) Evolutionary quantitative genetics. Chapman and Hall, New YorkGoogle Scholar
  71. Sober E (1988) Reconstructing the past: parsimony, evolution, and inference. MIT Press, CambridgeGoogle Scholar
  72. Storz JF, Beaumont MA, Alberts SC (2002) Genetic evidence for long-term population decline in a savannah-dwelling primate: Inferences from a hierarchical Bayesian model. Mol Biol Evol 19:1981–1990PubMedGoogle Scholar
  73. van Schaik CP, Kappeler PM (1996) The social systems of gregarious lemurs: lack of convergence with anthropoids due to evolutionary disequilibrium? Ethology 102:915–941CrossRefGoogle Scholar
  74. Virah-Swamy M, Gillson L, Willis KJ (2009) How does spatial heterogeneity influence resilience to climatic changes? Ecology dynamics in southeast Madagascar. Ecol Monogr 79:557–574CrossRefGoogle Scholar
  75. Vucetich JA, Waite TA, Nunney L (1997) Fluctuating population size and the ratio of effective to census population size. Evolution 51:2017–2021CrossRefGoogle Scholar
  76. Wroe S, Field J, Grayson DK (2006) Megafaunal extinction: climate, humans and assumptions. Trends Ecol Evol 21:61–62CrossRefPubMedGoogle Scholar
  77. Yoder AD, Nowak MD (2006) Has vicariance or dispersal been the predominant biogeographic force in Madagascar? Only time will tell. Annu Rev Ecol Syst 37:405–431CrossRefGoogle Scholar
  78. Yoder AD, Burns MM, Zehr S, Delefosse T, Veron G, Goodman SM, Flynn JJ (2003) Single origin of Malagasy carnivora from an African ancestor. Nature 421:734–737CrossRefPubMedGoogle Scholar
  79. Zhang B, Li M, Zhang Z, Goosens B, Zhu L, Zhang S, Hu J, Bruford MW, Wei F (2007) Genetic viability and population history of the giant panda, putting an end to the “evolutionary dead end?”. Mol Biol Evol 24:1801–1810CrossRefPubMedGoogle Scholar

Copyright information

© The Society of Population Ecology and Springer 2010

Authors and Affiliations

  1. 1.Anthropology DepartmentJames Madison UniversityHarrisonburgUSA

Personalised recommendations