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Bridging the gaps between non-invasive genetic sampling and population parameter estimation

Abstract

Reliable estimates of population parameters are necessary for effective management and conservation actions. The use of genetic data for capture–recapture (CR) analyses has become an important tool to estimate population parameters for elusive species. Strong emphasis has been placed on the genetic analysis of non-invasive samples, or on the CR analysis; however, little attention has been paid to the simultaneous overview of the full non-invasive genetic CR analysis, and the important insights gained by understanding the interactions between the different parts of the technique. Here, we review the three main steps of the approach: designing the appropriate sampling scheme, conducting the genetic lab analysis, and applying the CR analysis to the genetic results; and present a synthesis of this topic with the aim of discussing the primary limitations and sources of error. We discuss the importance of the integration between these steps, the unique situations which occur with non-invasive studies, the role of ecologists and geneticists throughout the process, the problem of error propagation, and the sources of biases which can be present in the final estimates. We highlight the importance of team collaboration and offer a series of recommendations to wildlife ecologists who are not familiar with this topic yet but may want to use this tool to monitor populations through time.

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References

  • Adams J, Kelly B, Waits L (2003) Using faecal DNA sampling and GIS to monitor hybridization between red wolves (Canis rufus) and coyotes (Canis latrans). Mol Ecol 12:2175–2186

    CAS  Article  PubMed  Google Scholar 

  • Ayres KL, Overall ADJ (2004) api-calc 1.0: a computer program for calculating the average probability of identity allowing for substructure, inbreeding and the presence of close relatives. Mol Ecol Notes 4:315–318

    CAS  Article  Google Scholar 

  • Begon M (1983) Abuses of mathematical techniques in ecology: applications of Jolly's capture-recapture method. Oikos 40:155–158

    Article  Google Scholar 

  • Bonin A, Bellemain E, Bronken Eidesen P, Pompanon F, Brochmann C, Taberlet P (2004) How to track and assess genotyping errors in population genetics studies. Mol Ecol 13:3261–3273

    CAS  Article  PubMed  Google Scholar 

  • Boulanger J, McLellan BN (2001) Closure violation in DNA-based mark-recapture estimation of grizzly bear populations. Can J Zool 79:642–651

    Article  Google Scholar 

  • Boulanger J, McLellan BN, Woods JG, Proctor M, Strobeck C (2004) Sampling design and bias in DNA-based capture-mark-recapture population and density estimates of grizzly bears. J Wildl Manage 68:457–469

    Article  Google Scholar 

  • Boulanger J, Proctor M, Himmer S, Stenhouse G, Paetkau D, Cranston J (2006) An empirical test of DNA mark-recapture sampling strategies for grizzly bears. Ursus 17:149–158

    Article  Google Scholar 

  • Broquet T, Petit E (2004) Quantifying genotyping errors in noninvasive population genetics. Mol Ecol 13:3601–3608

    CAS  Article  PubMed  Google Scholar 

  • Broquet T, Menard N, Petit E (2007) Noninvasive population genetics: a review of sample source, diet, fragment length and microsatellite motif effects on amplification success and genotyping error rates. Conserv Genet 8:249–260

    Article  Google Scholar 

  • Budowle B, Eisenberg AJ, VanDaal A (2009) Validity of Low Copy Number Typing and Applications to Forensic Science. Croat Med J 50:207–217

    CAS  Article  PubMed  Google Scholar 

  • Creel S, Spong G, Sands J, Rotella J, Zeigle J, Joe L, Murphy KM, Smith DLJ (2003) Population size estimation in Yellowstone wolves with error-prone noninvasive microsatellite genotypes. Mol Ecol 12:2003–2009

    Article  PubMed  Google Scholar 

  • Cubaynes S, Pradel R, Choquet R, Duchamp C, Gaillard J, Lebreton J, Marboutin E, Miquel C, Reboulet A, Poillot C, Taberlet P, Gimenez O (2010) Importance of accounting for detection heterogeneity when estimating abundance: the case of French Wolves. Conserv Biol 24:621–626

    Article  PubMed  Google Scholar 

  • Dematteo K, Rinas M, Sede M, Davenport B, Arguelles C, Lovett K, Parker P (2009) Detection dogs: an effective technique for bush dog surveys. J Wildl Manage 73:1436–1440

    Article  Google Scholar 

  • DeYoung RW, Brennan LA (2005) Molecular genetics in wildlife science, conservation, and management. J Wildl Manage 69:1360–1361

    Article  Google Scholar 

  • Ebert C, Huckschlag D, Schulz HK, Hohmann U (2009) Can hair traps sample wild boar (Sus scrofa) randomly for the purpose of non-invasive population estimation? Eur J Wildl Res 56:583–590

    Article  Google Scholar 

  • Eggert LS, Eggert JA, Woodruff DS (2003) Estimating population sizes for elusive animals: the forest elephants of Kakum National Park, Ghana. Mol Ecol 12:1389–1402

    CAS  Article  PubMed  Google Scholar 

  • Flagstad O, Hedmark E, Landa A, Broseth H, Persson J, Andersen R, Segerstrom P, Ellegren H (2004) Colonization history and noninvasive monitoring of a reestablished wolverine population. Conserv Biol 18:676–688

    Article  Google Scholar 

  • Frantz AC, Roper TJ (2006) Simulations to assess the performance of different rarefaction methods in estimating population size using small datasets. Conserv Genet 7:315–318

    Article  Google Scholar 

  • Gazey WJ, Staley MJ (1986) Population estimation from mark-recapture experiments using a sequential Bayes algorithm. Ecology 67:941–951

    Article  Google Scholar 

  • Gleeson DM, Byrom AE, Howitt RLJ (2010) Non-invasive methods for genotyping of stoats (Mustela erminea) in New Zealand: potential for field applications. NZ J Ecol 34:000–000

    Google Scholar 

  • Guschanski K, Vigilant L, McNeilage A, Gray M, Kagoda E, Robbins M (2009) Counting elusive animals: comparing field and genetic census of the entire mountain gorilla population of Bwindi Impenetrable National Park, Uganda. Biol Conserv 142:290–300

    Article  Google Scholar 

  • Jacob GR, Debrunner F, Gugerli B, Schmid BK (2010) Field surveys of capercaillie (Tetrao urogallus) in the Swiss Alps underestimated local abundance of the species as revealed by genetic analyses of non-invasive samples. Conserv Genet 11:33–44

    Article  Google Scholar 

  • Kalinowski ST, Wagner AP, Taper M (2006) ML-RELATE: a computer program for maximum likelihood estimation of relatedness and relationship. Mol Ecol Notes 6:576–579

    CAS  Article  Google Scholar 

  • Kendall KC, Stetz JB, Boulanger J, Macleod AC, Paetkau D, White GC (2009) Demography and genetic structure of a recovering grizzly bear population. J Wildl Manage 73:3–17

    Article  Google Scholar 

  • Knapp S, Craig B, Waits L (2009) Incorporating genotyping error into non-invasive DNABased Mark–Recapture Population Estimates. J Wildl Manage 73(4):598–604

    Article  Google Scholar 

  • Kohn MH, York EC, Kamradt DA, Haught G, Sauvajot RM, Wayne R (1999) Estimating population size by genotyping faeces. Proc R Soc Lond ser B 266:657–663

    CAS  Article  Google Scholar 

  • Lebreton J-D, Pradel R (2002) Multistate recapture models: modelling incomplete individual histories. J Appl Stat 29:353–369

    Article  Google Scholar 

  • Lebreton J-D, Burnham KP, Clobert J, Anderson DR (1992) Modeling survival and testing biological hypoyhesis using marked animals: a unified approach with case studies. Ecol Monogr 62:67–118

    Article  Google Scholar 

  • Lebreton J-D, Pradel R, Clobert J (1993) The statistical analysis of survival in animal populations. Trends Ecol Evol 8:91–95

    CAS  Article  PubMed  Google Scholar 

  • Lucchini V, Fabbri E, Marucco F, Ricci S, Boitani L, Randi E (2002) Noninvasive molecular tracking of colonizing wolves (Canis lupus) packs in the Western Italian Alps. Mol Ecol 11:857–868

    CAS  Article  PubMed  Google Scholar 

  • Luikart G, Ryman N, Tallmon DA, Schwartz MK, Allendorf FW (2010) Estimation of census and effective population sizes: the increasing usefulness of DNA-based approaches. Conserv Genet 11:355–373

    CAS  Article  Google Scholar 

  • Lukacs PM (2005) Statistical aspects of using genetic markers for individual identification in capture-recapture studies. Ph.D. thesis, Colorado State University

  • Lukacs PM, Burnham KP (2005) Review of capture-recapture methods applicable to noninvasive genetic sampling. Mol Ecol 14:3909–3919

    Article  PubMed  Google Scholar 

  • MacKay P, Smith DA, Long RA, Parker M (2008) Scat detection dogs. In: Long RA (ed) Noninvasive survey methods for carnivores. Island Press, Washington, pp 183–222

    Google Scholar 

  • MacKenzie DI (2006) Modeling the probability of resource use: the effect of, and dealing with, detecting a species imperfectly. J Wildl Manage 70:367–374

    Article  Google Scholar 

  • Marucco F (2009) Spatial population dynamics of a recolonizing wolf population in the Western Alps. Ph.D. dissertation, University of Montana

  • Matejusová I, Doig F, Middlemas SJ, Mackay S, Douglas A, Armstrong JD, Cunningham CO, Snow M (2008) Using quantitative real-time PCR to detect salmonid prey in scats of grey Halichoerus grypus and harbour Phoca vitulina seals in Scotland—an experimental and field study. J Appl Ecol 45:632–640

    Article  Google Scholar 

  • McKelvey K, Schwartz MK (2004) Genetic errors associated with population estimation using non-invasive molecular tagging: problems and new solutions. J Wildl Manage 68:439–448

    Article  Google Scholar 

  • McKelvey K, Schwartz MK (2005) DROPOUT: a program to identify problem loci and samples for noninvasive genetic samples in a captutre-mark-recapture framework. Mol Ecol Notes 5:716–18

    CAS  Article  Google Scholar 

  • McKelvey K, Von Kienast J, Aubry KB, Koehler GM, Maletzke BT, Squires JR, Lindquist EL, Loch S, Schwartz MK (2006) DNA analysis and hair and scat collected along snow tracks to document the presence of Canada Lynx. Wildl Soc Bull 34:451–455

    Article  Google Scholar 

  • Miller CR, Joyce P, Waits LP (2002) Assessing allelic dropout and genotype reliability using maximum likelihood. Genetics 160:357–366

    PubMed  Google Scholar 

  • Miller CR, Joyce P, Waits LP (2005) A new method for estimating the size of small populations from genetic mark-recapture data. Ecology 14:1991–2005

    CAS  Google Scholar 

  • Mills LS, Citta JJ, Lair KP, Schwartz MK, Tallmon DA (2000) Estimating animal abundance using noninvasive DNA sampling: promise and pitfalls. Ecol Appl 10:283–294

    Article  Google Scholar 

  • Miquel C, Bellemain E, Poillot C, Bessière J, Durand A, Taberlet P (2006) Quality indexes to assess the reliability of genotypes in studies using noninvasive sampling and multiple-tube approach. Mol Ecol Notes 6:985–988

    Article  Google Scholar 

  • Morin P, Chambers K, Boesch C, Vigilant L (2001) Quantitative polymerase chain reaction analysis of DNA from noninvasive samples for accurate microsatellite genotyping of wild chimpanzees (Pan troglodytes verus). Mol Ecol 10:1835–1844

    CAS  Article  PubMed  Google Scholar 

  • Mowat G, Paetkau D (2002) Estimating marten (Martes americana) population size using hair capture and genetic tagging. Wildl Biol 8:201–209

    Google Scholar 

  • Mowat G, Strobeck C (2000) Estimating population size of grizzly bears using hair capture and genetic tagging. J Wildl Manage 64:183–193

    Article  Google Scholar 

  • Mulders R, Boulanger J, Paetkau D (2007) Estimation of population size for wolverines Gulo gulo at Daring Lake, Northwest territories, using DNA based mark-recapture methods. Wildl Biol 13:38–51

    Google Scholar 

  • Nichols JD (1992) Capture-recapture models: using marked animals to study population dynamics. Bioscience 42:94–102

    Article  Google Scholar 

  • O'Connell M, Wright JM (1997) Microsatellite DNA in fishes. Rev Fish Biol Fish 7:331–363

    Article  Google Scholar 

  • Paetkau D (2003) An empirical exploration of data quality in DNA-based population inventories. Mol Ecol 12:1375–1387

    CAS  Article  PubMed  Google Scholar 

  • Penacino G, Sala A, Corach D (2003) Are DNA tests infallible? Int Congr Ser 1239:873–877

    CAS  Article  Google Scholar 

  • Perkel J (2008) SNO genotyping: six technologies that keyed a revolution. Nat Meth 5:447–453

    CAS  Article  Google Scholar 

  • Petit E, Valiere N (2006) Estimating population size with noninvasive capture-mark-recapture data. Conserv Biol 20:1062–1073

    Article  PubMed  Google Scholar 

  • Pledger S, Efford M (1998) Correction of bias due to heterogeneous capture probability in capture-recapture studies of open populations. Biometrics 54:888–898

    Article  Google Scholar 

  • Pledger S, Pollock KH, Norris JL (2003) Open capture-recapture models with heterogeneity: I. Cormack–Jolly–Seber model. Biometrics 59:786–794

    Article  PubMed  Google Scholar 

  • Pollock KH, Nichols JD, Brownie C, Hines JE (1990) Statistical inference for capture-recapture experiments. Wildl Monogr 107:1–97

    Google Scholar 

  • Pompanon F, Bonin A, Bellemain E, Taberlet P (2005) Genotyping errors: causes, consequences and solutions. Nat Rev 6:847–859

    CAS  Article  Google Scholar 

  • Powell LA, Conroy M, Hines JE, Krementz DG (2000) Simultaneous use of mark-recapture and radiotelemetry to estimate survival, movement, and capture rates. J Wildl Manage 64:302–313

    Article  Google Scholar 

  • Pradel R, Hines JE, Lebreton J-D, Nichols JD (1997a) Capture-recapture survival models taking account of transients. Biometrics 53:60–72

    Article  Google Scholar 

  • Pradel R, Hines JE, Lebreton JD, Nichols JD (1997b) Estimating survival rate and proportion of transients using capture-recapture data from open populations. Biometrics 53:88–99

    Article  Google Scholar 

  • Prugh LR, Ritland CE, Arthur SM, Krebs CJ (2005) Monitoring coyote population dynamic by genotyping faeces. Mol Ecol 14:1585–1596

    CAS  Article  PubMed  Google Scholar 

  • Puechmaille SJ, Petit EJ (2007) Empirical evaluation of non-invasive capture-mark-recapture estimation of population size based on a single sampling session. J Appl Ecol 44:843–852

    Article  Google Scholar 

  • Roon DA, Waits LP, Kendall KC (2005) A simulation test of the effectiveness of several methods for error-checking non-invasive genetic data. Anim Conserv 8:203–215

    Article  Google Scholar 

  • Ruibal M, Peakall R, Claridge A, Firestone K (2009) Field-based evaluation of scat DNA methods to estimate population abundance of the spotted-tailed quoll (Dasyurus maculatus), a rare Australian marsupial. Wildl Res 36:721–736

    CAS  Article  Google Scholar 

  • Saks MJ, Koehler JJ (2005) The coming paradigm shift in forensic identification science. Science 309:892–895

    CAS  Article  PubMed  Google Scholar 

  • Saks MJ, Risinger DM, Rosenthal R, Thompson W (2003) Context effects in forensic science: a review and application of the science of science to crime laboratory practice in the United States. Sci Justice 43:77–90

    CAS  Article  PubMed  Google Scholar 

  • Schwartz MK, Monfort SL (2008) DNA and endocrine sampling. In: Long RA, MacKay P, Ray JC, Zielinski WJ (eds) Noninvasive survey methods for North American carnivores. Island Press, Washington

    Google Scholar 

  • Schwartz MK, Luikart G, Waples RS (2007) Genetic monitoring as a promising tool for conservation and management. Trends Ecol Evol 22:25–33

    Article  PubMed  Google Scholar 

  • Schwarz CJ, Stobo WT (1999) Estimation and effects of tag-misread rates in capture-recapture studies. Can J Fish Aquat Sci 56:551–559

    Article  Google Scholar 

  • Settlage KE, Van Manen FT, Clark JD, King TL (2008) Challenges of DNA-based mark-recapture studies of American Black Bears. J Wildl Manage 72:1035–1042

    Google Scholar 

  • Smith DA, Balls K, Cypher B, Maldonado JE (2005) Assessment of scat-detection dog surveys to determine kit fox distribution. Wildl Soc Bull 33:897–904

    Article  Google Scholar 

  • Smith DA, Ralls K, Hurt A, Adams B, Parker M, Maldonado JE (2006) Assessing reliability of microsatellite genotypes from kit fox faecal samples using genetic and GIS analysis. Mol Ecol 15:387–406

    CAS  Article  PubMed  Google Scholar 

  • Solberg KH, Bellemain E, Drageset O-M, Taberlet P, Swenson JE (2006) An evaluation of field and non-invasive genetic methods to estimate brown bear (Ursus arctos) population size. Biol Conserv 128:158–168

    Article  Google Scholar 

  • Stevick PT, Palsboll PJ, Smith TD, Bravington MV, Hammond PS (2001) Errors in identification using natural markings: rates, sources, and effects on capture-recapture estimates of abundance. Can J Fish Aquat Sci 58:1861–1870

    Article  Google Scholar 

  • Taberlet P, Griffin S, Goossens B, Questiau S, Manceau V, Escaravage N, Waits LP, Bouvet J (1996) Reliable genotyping of samples with very low DNA quantities using PCR. Nucleic Acids Res 26:3189–3194

    Article  Google Scholar 

  • Valiere N, Berthier P, Mouchiroud D, Pontier D (2002) GEMINI: software for testing the effects of genotyping errors and multitube approach for individual identification. Mol Ecol Notes 2:83–86

    CAS  Google Scholar 

  • Valiere N, Bonenfant C, Toigo C, Luikart G, Gaillard J-M, Klein F (2007) Importance of a pilot study for non-invasive genetic sampling: genotyping errors and population size estimation in red deer. Conserv Genet 8:69–78

    Article  Google Scholar 

  • Wagner AP, Creel S, Frank LG, Kalinowski ST (2007) Patterns of relatedness and parentage in an asocial, polyandrous striped hyena population. Mol Ecol 16:4356–4369

    CAS  Article  PubMed  Google Scholar 

  • Waits JL, Leberg PL (2000) Biases associated with population estimation using molecular tagging. Anim Conserv 3:191–199

    Article  Google Scholar 

  • Waits LP, Luikart G, Taberlet P (2001) Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Mol Ecol 10:249–256

    CAS  Article  PubMed  Google Scholar 

  • Wasser SK, Davenport B, Ramage ER, Hunt KE, Parker M, Clarke C, Stenhouse G (2004) Scat detection dogs in wildlife research and management: application to grizzly and black bears in the Yellowhead Ecosystem, Alberta, Canada. Can J Zool 82:475–492

    Article  Google Scholar 

  • White GC, Anderson DR, Burnham KP, Otis DL (1982) Capture-recapture and removal methods for sampling closed populations. Los Alamos National Laboratory, LA 8787-NERP, Los Alamos

    Google Scholar 

  • Williams BK, Nichols JD, Conroy MJ (2002) Analysis and management of animal populations. Academic, San Francisco

    Google Scholar 

  • Wilson GJ, Frantz AC, Pope LC, Roper TJ, Burke TA, Cheeseman CL, Delahay RJ (2003) Estimation of badger abundance using faecal DNA typing. J Appl Ecol 40:658–666

    Article  Google Scholar 

  • Wright JA, Barker RJ, Schofield MR, Frantz AC, Byrom AE, Gleeson DM (2009) Incorporating genotyping uncertainty into mark-recapture-type models for estimating abundance using DNA samples. Biometrics 65:833–840

    CAS  Article  PubMed  Google Scholar 

  • Yoshizaki J (2007) Use of natural tags in closed population capture-recapture studies: modelling misidentification. Dissertation, North Carolina State University

  • Zhan X, Li M, Zhang Z, Goossens B, Chen Y, Wang H, Bruford MW, Wei F (2006) Molecular censusing doubles giant panda population estimate in a key nature reserve. Curr Biol 16:R451–R452

    CAS  Article  PubMed  Google Scholar 

  • Zielinski WJ, Schlexer FV, Pilgrim KL, Schwartz MK (2006) Testing the efficacy of two methods for snaring hair from mesocarnivores. Wildl Soc Bull 34:1152–1161

    Article  Google Scholar 

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Acknowledgements

We thank K. Griffin, P. Ciucci, and J. Boulanger for helpful comments on the first draft of this paper. F. Marucco was supported by the Regione Piemonte, Progetto Lupo Piemonte, Parco Naturale Alpi Marittime. M. Schwartz was supported by a PECASE award during the writing of this manuscript.

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Correspondence to Francesca Marucco.

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Communicated by C. Gortázar.

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Marucco, F., Boitani, L., Pletscher, D.H. et al. Bridging the gaps between non-invasive genetic sampling and population parameter estimation. Eur J Wildl Res 57, 1–13 (2011). https://doi.org/10.1007/s10344-010-0477-7

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  • DOI: https://doi.org/10.1007/s10344-010-0477-7

Keywords

  • Capture-mark-recapture
  • Genetic
  • Molecular tagging
  • Non-invasive
  • Population size