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
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
Begon M (1983) Abuses of mathematical techniques in ecology: applications of Jolly's capture-recapture method. Oikos 40:155–158
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
Boulanger J, McLellan BN (2001) Closure violation in DNA-based mark-recapture estimation of grizzly bear populations. Can J Zool 79:642–651
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
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
Broquet T, Petit E (2004) Quantifying genotyping errors in noninvasive population genetics. Mol Ecol 13:3601–3608
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
Budowle B, Eisenberg AJ, VanDaal A (2009) Validity of Low Copy Number Typing and Applications to Forensic Science. Croat Med J 50:207–217
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
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
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
DeYoung RW, Brennan LA (2005) Molecular genetics in wildlife science, conservation, and management. J Wildl Manage 69:1360–1361
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
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
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
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
Gazey WJ, Staley MJ (1986) Population estimation from mark-recapture experiments using a sequential Bayes algorithm. Ecology 67:941–951
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
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
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
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
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
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
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
Lebreton J-D, Pradel R (2002) Multistate recapture models: modelling incomplete individual histories. J Appl Stat 29:353–369
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
Lebreton J-D, Pradel R, Clobert J (1993) The statistical analysis of survival in animal populations. Trends Ecol Evol 8:91–95
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
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
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
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
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
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
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
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
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
Miller CR, Joyce P, Waits LP (2002) Assessing allelic dropout and genotype reliability using maximum likelihood. Genetics 160:357–366
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
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
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
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
Mowat G, Paetkau D (2002) Estimating marten (Martes americana) population size using hair capture and genetic tagging. Wildl Biol 8:201–209
Mowat G, Strobeck C (2000) Estimating population size of grizzly bears using hair capture and genetic tagging. J Wildl Manage 64:183–193
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
Nichols JD (1992) Capture-recapture models: using marked animals to study population dynamics. Bioscience 42:94–102
O'Connell M, Wright JM (1997) Microsatellite DNA in fishes. Rev Fish Biol Fish 7:331–363
Paetkau D (2003) An empirical exploration of data quality in DNA-based population inventories. Mol Ecol 12:1375–1387
Penacino G, Sala A, Corach D (2003) Are DNA tests infallible? Int Congr Ser 1239:873–877
Perkel J (2008) SNO genotyping: six technologies that keyed a revolution. Nat Meth 5:447–453
Petit E, Valiere N (2006) Estimating population size with noninvasive capture-mark-recapture data. Conserv Biol 20:1062–1073
Pledger S, Efford M (1998) Correction of bias due to heterogeneous capture probability in capture-recapture studies of open populations. Biometrics 54:888–898
Pledger S, Pollock KH, Norris JL (2003) Open capture-recapture models with heterogeneity: I. Cormack–Jolly–Seber model. Biometrics 59:786–794
Pollock KH, Nichols JD, Brownie C, Hines JE (1990) Statistical inference for capture-recapture experiments. Wildl Monogr 107:1–97
Pompanon F, Bonin A, Bellemain E, Taberlet P (2005) Genotyping errors: causes, consequences and solutions. Nat Rev 6:847–859
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
Pradel R, Hines JE, Lebreton J-D, Nichols JD (1997a) Capture-recapture survival models taking account of transients. Biometrics 53:60–72
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
Prugh LR, Ritland CE, Arthur SM, Krebs CJ (2005) Monitoring coyote population dynamic by genotyping faeces. Mol Ecol 14:1585–1596
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
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
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
Saks MJ, Koehler JJ (2005) The coming paradigm shift in forensic identification science. Science 309:892–895
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
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
Schwartz MK, Luikart G, Waples RS (2007) Genetic monitoring as a promising tool for conservation and management. Trends Ecol Evol 22:25–33
Schwarz CJ, Stobo WT (1999) Estimation and effects of tag-misread rates in capture-recapture studies. Can J Fish Aquat Sci 56:551–559
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
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
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
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
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
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
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
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
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
Waits JL, Leberg PL (2000) Biases associated with population estimation using molecular tagging. Anim Conserv 3:191–199
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
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
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
Williams BK, Nichols JD, Conroy MJ (2002) Analysis and management of animal populations. Academic, San Francisco
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
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
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
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
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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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