Conservation Genetics

, Volume 16, Issue 5, pp 1167–1180 | Cite as

Estimating effective population size of guanacos in Patagonia: an integrative approach for wildlife conservation

  • Ronald J. SarnoEmail author
  • David E. Jennings
  • William L. Franklin
Research Article


By the mid-1900s the guanaco (Lama guanicoe) approached extinction in southern South America due to habitat destruction and hunting. In order to maintain the ecological prominence of this iconic species, as well as assist in the management of populations that are emerging economically while increasing in conservation value, accurate and potentially rapid estimates of effective population size (Ne) (demographic and/or genetic) are essential. Estimates of Ne generally focus on the genetic effective population size; however, we posited that both parameters may be necessary to provide more accurate and timely estimates. Therefore, we examined the performance of three demographic and four genetic estimators of Ne of guanacos in Torres del Paine National Park, Chile, at different years and time intervals between 1987 and 1997. We compared our estimates with census estimates of the adult population size (Nac) during the same time period. Average Ne/Nac ratios of demographic estimates varied between 0.04 and 0.99 of the adult census size. Genetic estimates varied between 0.02 and 0.08 of the adult census size. Based upon group composition and population size (n = 82) of guanacos in 1975, the number of breeding adults was 44 animals. Mean Ne of the single-sample and temporal genetic estimators was 43.1, and 34.3, respectively; estimated Ne of one of the demographic estimators was 41. Our findings suggest that intermittent genetic estimates of Ne (via fecal samples, carcasses, blood collection during capture, and/or other non-invasive methods) can provide crucial information regarding the genetic integrity of increasingly isolated populations of wild South American camelids. Considering the overall performance of these estimators, and differences in how each functions, we recommend an integrative approach using both genetic and demographic estimators, to evaluate Ne for the wild South American camelids and other species with polygynous mating systems.


Conservation genetics Lama guanicoe Camelids Effective population size Patagonia Polygynous mating systems 



We thank the Chilean National Forestry and Park Service (CONAF), and the administration at Torres del Paine National Park, particularly Guillermo Santana, Juan Toro and Nicolás Soto. Dr. Russ Hunter DVM, Jan Marts, Brian Soppe, Dick Schmits, Mike Behl, Beth Behl, Tina Chladny, John Reed, Carrie Bergman, Kari Stueckrath, John Rathje, Tim Sulser, Stephanie Shoemaker, Dr. Kathryn Guderian DVM, Eric and Kim Gaylord, Kelly Nielsen, Anne Engh, Paul Heaven, Irene O’Connell, Walter Prexl, Mike Bank, Warren Johnson, and the participants of Patagonia Research Expeditions assisted in blood collection. Michael Parsons and Al Roca provided helpful comments on previous versions of the MS. Pierre Berthier, Jinlian Wang provided insight into the use of TM3 and MLNE. Robin Waples and David Tallmon answered numerous questions regarding program performance and statistical inference for LDNe and ONeSAMP, respectively. Richard Trapmore wrote the code in C# and Evan Carson provided suggestions how to structure simulations. Two anonymous reviewers also provided many useful suggestions. Capture, handling and blood exportation permits were issued by Servicio Agricola y Ganadero (SAG). Permits to import blood samples into the US were issued by the USDA to Ronald J. Sarno. This study was supported by Patagonia Research Expeditions, National Science Foundation Grant No. BSR-9112826, and Organization of American States Grant No. 19104.


  1. Alò D, Turner TF (2005) Effects of habitat fragmentation on effective population size in the endangered Rio Grande silvery minnow. Conserv Biol 19:1138–1148CrossRefGoogle Scholar
  2. Baldi R, Novaro A, Funes M, Walker S, Ferrando P, Failla M, Carmanchahi P (2010) Guanaco management in patagonian rangelands: a conservation opportunity on the brink of collapse. Wild rangelands: conserving wildlife while maintaining livestock. In: du Toit JT, Kock R, Deutsch JC (eds) Semi-arid ecosystems, 1st edn. Blackwell Publishing, London, pp 266–290Google Scholar
  3. Berthier P, Beaumont MA, Cornuet JM, Luikart G (2002) Likelihood-based estimation of the effective population size using temporal changes in allele frequencies: a genealogical approach. Genetics 160:741–751PubMedCentralPubMedGoogle Scholar
  4. Bidinost F, Roldan DL, Dodero AM, Cano EM, Taddeo HR, Mueller JP, Poli MA (2008) Wool quantitative trait loci in Merino Sheep. Small Rumin Res 74:113–118CrossRefGoogle Scholar
  5. Bishop JM, Leslie AJ, Bourquin SL, O’Ryan C (2009) Reduced effective population size in an overexploited population of the Nile crocodile (Crocodylus niloticus). Biol Conserv 142:2335–2341CrossRefGoogle Scholar
  6. Cano EM, Marrube G, Roldan DL, Bidinost F, Abad M, Allain D, Vaiman D, Taddeo H, Poli MA (2007) QTL affecting fleece traits in Angora goats. Small Rumin Res 71:158–164CrossRefGoogle Scholar
  7. Caughley G (1977) Analysis of vertebrate populations. Wiley, New YorkGoogle Scholar
  8. Cronin MA, Amstrup SC, Talbot SL, Sage GK, Amstrup KS (2009) Genetic variation, relatedness, and effective population size of polar bears (Ursus maritimus) in the southern Beaufort Sea, Alaska. J Hered 100:681–690CrossRefPubMedGoogle Scholar
  9. Crow JF, Kimura M (1970) An introduction to population genetics theory. Harper & Rowe, New YorkGoogle Scholar
  10. Dennler de la Tour G (1954) The guanaco. Oryx 2:273–279CrossRefGoogle Scholar
  11. Easteal S (1985) The ecological genetics of introduced populations of the giant toad Bufo marinus. II. Effective population size. Genetics 110:107–122PubMedCentralPubMedGoogle Scholar
  12. Frank EN, Hick MVH, Gauna CD, Lama HE, Renieri C, Antonini M (2006) Phenotypic and genetic description of fibre traits in South American domestic camelids (llamas and alpacas). Small Rumin Res 61:113–129CrossRefGoogle Scholar
  13. Frankham R (2005) Genetics and extinction. Biol Conserv 126(2005):131–140CrossRefGoogle Scholar
  14. Frankham R, Ballou JD, Briscoe DA (2010) Introduction to Conservation Genetics. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  15. Franklin WL (1982) Biology, ecology, and relationship to man of the South American camelids. Spec Publ Pymatuning Lab Ecol 6:457–489Google Scholar
  16. Franklin WL (2011) Family Camelidae (camels). In: Wilson DE, Mittermeier RA (eds) Handbook of the mammals of the world, vol 2., Hoofed MammalsLynx Ediciones, Barcelona, pp 206–246Google Scholar
  17. Franklin WL, Fritz MA (1991) Sustained harvesting of the Patagonia guanaco: is it possible or too late? In: Robinson JG, Redford KH (eds) Neotropical wildlife use and conservation. University of Chicago Press, Chicago, pp 317–336Google Scholar
  18. Franklin WL, Grigione MM (2005) The enigma of guanacos in the Falkland Islands: the legacy of John Hamilton. J Biogeogr 32:661–675CrossRefGoogle Scholar
  19. Franklin W, Bas FM, Bonacic CF, Cunazza CP, Soto VN (1997) Striving to manage Patagonia guanacos for sustained use in the grazing agroecosystems of southern Chile. Wildl Soc Bull 25:65–73Google Scholar
  20. Gaillard J-M, Festa-Bianchet M, Yoccoz NG (1998) Population dynamics of large herbivores: variable recruitment with constant adult survival. TREE 13:58–63PubMedGoogle Scholar
  21. González BA, Orozco-terWelgel P, von Borries R, Johnson WE, Marín JC (2014) Maintenance of genetic diversity in an introduced island population of guanacos after seven decades and two severe demographic bottlenecks: implications for camelid conservation. PLoS One. doi: 10.1371/journal.pone.0091714 Google Scholar
  22. Gordon IJ (2009) The philosophy of sustainable wildlife use. In: Gordon IJ (ed) The vicuna-the theory and practice of community based wildlife management. Springer, Townsville, pp 1–6Google Scholar
  23. Guo S, Thompson E (1992) Performing the exact test of Hardy–Weinberg proportion for multiple alleles. Biometrics 48:361–372CrossRefPubMedGoogle Scholar
  24. Henry P, Miquelle D, Sugimoto T, McCullough DR, Caccone A, Russello MA (2009) In situ population structure and ex situ representation of the endangered Amur tiger. Mol Ecol 18:3173–3184CrossRefPubMedGoogle Scholar
  25. Hoehn M, Gruber B, Sarre SD, Lange R, Henle K (2012) Can genetic estimators provide robust estimates of the effective number of breeders in small populations? PLoS One. doi: 10.1371/journal.pone.0048464 Google Scholar
  26. Hoffman EA, Schueler FW, Blouin MS (2004) Effective population sizes and temporal stability of genetics structure in Rana pipiens, the northern leopard frog. Evolution 58:2536–2545CrossRefPubMedGoogle Scholar
  27. Howard WE (1970) Relationship of wildlife to sheep husbandry in Patagonia, Argentina. FAO Rep 14:1–31Google Scholar
  28. Jorde PE, Ryman N (1995) Temporal allele frequency change and estimation of effective size in populations with overlapping generations. Genetics 139:1077–1090PubMedCentralPubMedGoogle Scholar
  29. Jurgensen TE (1985) Seasonal territoriality in a migratory guanaco population. MS Thesis, Iowa State UniversityGoogle Scholar
  30. Kaeuffer R, Coltman DW, Chapuis JL, Réale D, Pontier D (2007) The effects of cyclic dynamics and mating system on the effective size of an island mouflon population. Mol Ecol 16:4482–4492CrossRefPubMedGoogle Scholar
  31. Leberg PL (2002) Estimating allelic richness: effects of sample size and bottlenecks. Mol Ecol 11:2445–2449CrossRefPubMedGoogle Scholar
  32. Lichtenstein G (2010) Current challenges for addressing vicuña conservation and poverty alleviation via vicuña management in Andean countries. Biodiversity 1&2:19–24CrossRefGoogle Scholar
  33. Lichtenstein G, Renaudeau d´Arc N (2008) Retórica y praxis de la participación local en los proyectos de manejo de vicuñas. Cuadernos XXI del Instituto de Antropología y Pensamiento Latinoamericano 21:133–141Google Scholar
  34. Luikart G, Ryman N, Tallmon DA, Schwartz MK, Allendorf FW (2010) Estimation of census effective population sizes: the increasing usefulness of DNA-based approaches. Conserv Genet 11:355–373CrossRefGoogle Scholar
  35. Miller LM, Kapuscinski AR (1997) Historical analysis of genetic variation reveals low effective population size in northern pike (Esox lucius) population. Genetics 147:1249–1258PubMedCentralPubMedGoogle Scholar
  36. Montes MC, Carmanchahi PD, Rey A, Funes MC (2006) Live-shearing free-ranging guanacos (Lama guanicoe) in Patagonia for sustainable use. J Arid Environ 64:616–625CrossRefGoogle Scholar
  37. Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10CrossRefGoogle Scholar
  38. Newman D, Pilson D (1997) Increased probability of extinction due to decreased genetic effective population size: experimental populations of Clarkia pulchella. Evolution 51:354–362CrossRefGoogle Scholar
  39. Novaro AJ, Funes MC, Walker RS (2000) Ecological extinction of native prey of a carnivore assemblage in Argentine Patagonia. Biol Cons 92:25–33CrossRefGoogle Scholar
  40. Nunney L (2002) The effective size of annual plant populations: the interaction of a seed bank with fluctuating plant numbers. Am Nat 160:195–204CrossRefPubMedGoogle Scholar
  41. Nunney L, Elam DR (1994) Estimation the effective population size of conserved populations. Conserv Biol 8:175–184CrossRefGoogle Scholar
  42. Ortega IM, Franklin WL (1988) Feeding habitat utilization and preference by guanaco male groups in the Chilean Patagonia. Rev Chi Hist Nat 61:209–216Google Scholar
  43. Palstra FP, Ruzzante DE (2008) Genetic estimates of contemporary effective population size: what can they tell us about the importance of genetic stochasticity for wild population persistence? Mol Ecol 17:3428–3447CrossRefPubMedGoogle Scholar
  44. Peng B, Amos CI (2008) Forward-time simulations of non-random mating populations using simuPOP. Bioinformatics 24:1408–1409CrossRefPubMedCentralPubMedGoogle Scholar
  45. Peng B, Kimmel M (2005) simuPOP: a forward-time population genetics simulation environment. Bioinformatics 21:3686–3687CrossRefPubMedGoogle Scholar
  46. Pisano E (1974) Estudio ecológico de la region continental sur del area andino-patagónica, II. Contribucion a la fitogeografia de la zona del parque Nacional “Torres del Paine”. Anales Instituto Patagonia (Chile) 5:59–104Google Scholar
  47. Poulsen NA, Nielsen EE, Schierup MH, Loeschcke V, Grønkjær P (2006) Long-term stability and effective population size in North Sea and Baltic Sea cod (Gadus morhua). Mol Ecol 15:321–331CrossRefPubMedGoogle Scholar
  48. Raedeke KJ (1979) Population dynamics and socioecology of the guanaco (Lama guanicoe) of Magallanes, Chile. Dissertation, University of WashingtonGoogle Scholar
  49. Reed DH (2005) Relationship between population size and fitness. Conserv Biol 19:563–568CrossRefGoogle Scholar
  50. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  51. Robinson JD, Moyer GR (2012) Linkage disequilibrium and effective population size when generations overlap. Evol Appl 6:290–302CrossRefPubMedCentralPubMedGoogle Scholar
  52. Rowe G, Beebee TJC (2004) Defining population boundaries: use of three Bayesian approaches with microsatellite data from British natterjack toads (Bufo calamita). Mol Ecol 16:785–796CrossRefGoogle Scholar
  53. Saccherri I, Kuussaari M, Kankare M, Vikman P, Fortelius W, Hanski I (1998) Inbreeding and extinction in a butterfly metapopulation. Nature 392:491–494CrossRefGoogle Scholar
  54. Sarno RJ, Franklin WL (1999) Population density and annual variation in birth mass of guanacos in southern Chile. J Mammal 80:1158–1162CrossRefGoogle Scholar
  55. Sarno RJ, Franklin WL, O’Brien SJ, Johnson WE (2001) Patterns of mtDNA and microsatellite variation in an island and mainland population of guanacos in southern Chile. Anim Conserv 4:93–101CrossRefGoogle Scholar
  56. Schmeller DS, Merilä J (2007) Demographic and genetic estimates of effective population and breeding size in the amphibian Rana temporaria. Conserv Biol 21:142–151CrossRefPubMedGoogle Scholar
  57. Scribner KT, Arntzen JW, Burke T (1997) Effective number of breeding adults in Bufo bufo estimated from age-specific variation at minisatellite loci. Mol Ecol 6:701–712CrossRefPubMedGoogle Scholar
  58. Soulé ME, Mills LS (1998) Population genetics: no need to isolate genetics. Science 282:1658–1659CrossRefGoogle Scholar
  59. Storz JF, Bhat HR, Kunz TR (2001) Genetic consequences of polygyny and social structure in an Indian fruit bat, Cynopterus sphinx. II. Variance in mate mating success and effective population size. Evolution 55:1224–1232CrossRefPubMedGoogle Scholar
  60. Tallmon DA, Koyuk A, Luikart G, Beaumont MA (2008) ONeSAMP: a program to estimate effective population size using approximate Bayesian computation. Mol Ecol Res 8:299–301CrossRefGoogle Scholar
  61. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-Checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  62. Veliz C, Hoces D (2008) Distribución potencial del guanaco y la vicuña en el Perú. In: Damonte G, Fulcrand B, Gomez R (eds) Libro SEPIA XII, Perú: el problema agrario en debate. Lima, pp 375–396Google Scholar
  63. Wang J, Whitlock MC (2003) Estimating effective population size and migration rates from genetic samples over space and time. Genetics 163:429–446PubMedCentralPubMedGoogle Scholar
  64. Waples RS (2005) Genetic estimates of contemporary effective population size: to what time periods do the estimates apply? Mol Ecol 14:3335–3352CrossRefPubMedGoogle Scholar
  65. Waples RS, Do C (2008) L d N e: a program for estimating effective population size from data on linkage disequilibrium. Mol Ecol Notes 8:753–756CrossRefGoogle Scholar
  66. Waples R, Yokota M (2007) Temporal estimates of effective population size in species with overlapping generations. Genetics 175:219–233CrossRefPubMedCentralPubMedGoogle Scholar
  67. Waples RS, Luikart G, Faulkner JR, Tallmon DA (2013) Simple life-history traits explain key effective population size ratios across diverse taxa. Proc R Soc B 280:20131339CrossRefPubMedCentralPubMedGoogle Scholar
  68. Waples R, Tiago A, Liukart G (2014) Effects of overlapping generations on linkage disequilibrium estimates of effective population size. Genetics. doi: 10.1534/genetics.114.164822 PubMedCentralPubMedGoogle Scholar
  69. Willi Y, Van Buskirk J, Hoffmann AA (2006) Limits to the adaptive potential of small populations. Annu Rev Ecol Evol Syst 37:433–458CrossRefGoogle Scholar
  70. Wright S (1931) Evolution in Mendelian populations. Genet 16:97–159Google Scholar
  71. Wright S (1938) Size of population and breeding structure in relation to evolution. Science 87:430–431Google Scholar
  72. Young JK, Franklin WL (2004) Territorial fidelity of male guanacos in the Patagonia of southern Chile. J Mammal 65:72–78CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Ronald J. Sarno
    • 1
    Email author
  • David E. Jennings
    • 2
  • William L. Franklin
    • 3
  1. 1.Department of Biology114 Hofstra UniversityHempsteadUSA
  2. 2.Department of EntomologyUniversity of MarylandCollege ParkUSA
  3. 3.Department of Animal EcologyIowa State UniversityAmesUSA

Personalised recommendations