Section: Ecology
Topic: Ecology, Population biology

Estimating abundance of a recovering transboundary brown bear population with capture-recapture models

Corresponding author(s): Vanpé, Cécile (cecile.vanpe@ofb.gouv.fr)

10.24072/pcjournal.199 - Peer Community Journal, Volume 2 (2022), article no. e71.

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Estimating the size of small populations of large mammals can be achieved via censuses, or complete counts, of recognizable individuals detected over a time period: minimum detected (population) size (MDS). However, as a population grows larger and its spatial distribution expands, the risk of under-estimating population size using MDS rapidly increases because the assumption of perfect detection of all individuals in the population is violated. The need to report uncertainty around population size estimates consequently becomes crucial. We explored these biases using the monitoring framework of the critically endangered Pyrenean brown bear that was close to extinction in the mid-1990s, with only five individuals remaining, but was subsequently bolstered by the introduction of 11 bears from Slovenia. Each year since 1996, the abundance of the population has been assessed using MDS and minimum retained (population) size (MRS), which corresponded to a reassessment of the MDS in the light of the new information collected in subsequent years (e.g., adding bears which were not detected the previous years but detected the current year). We used Pollock’s closed robust design (PCRD) capture-recapture models applied to the cross-border non-invasive sampling data from France, Spain and Andorra to provide the first published annual abundance and temporal trend estimates of the Pyrenean brown bear population since 2008. Annual population size increased fivefold between 2008 and 2020, going from 13 to 66 individuals. PCRD estimates were globally close to MRS counts and had reasonably narrow associated 95% Credibility Intervals. Even in cases where sampling effort is large compared to population size, the PCRD estimates of population size can diverge from the MDS counts. We report individual heterogeneity in detection that might stem from intraspecific home range size variation that result in individuals that move the most being most likely to be detected. We also found that cubs had a higher mortality rate than adults and subadults, because of infanticide by males, predation, maternal death, or abandonment. Overall, the PCRD capture-recapture modelling approach provides estimates of abundance and demographic rates of the Pyrenean brown bear population, together with associated uncertainty, while minimizing bias due to inter-individual heterogeneity in detection probabilities. We strongly encourage wildlife ecologists and managers to use robust approaches when researching large mammal populations. Such information is vital for informing management decision-making and assessing population conservation status.

Published online:
DOI: 10.24072/pcjournal.199
Type: Research article

Vanpé, Cécile 1; Piédallu, Blaise 2; Quenette, Pierre-Yves 1; Sentilles, Jérôme 1; Queney, Guillaume 3; Palazón, Santiago 4; Jordana, Ivan Afonso 5; Jato, Ramón 6; Irurtia, Miguel Mari Elósegui 7; de la Torre, Jordi Solà 8; Gimenez, Olivier 2

1 Direction de la Recherche et de l’Appui Scientifique (DRAS), Office Français de la Biodiversité (OFB) – Villeneuve-de-Rivière, France
2 Centre d’Ecologie Fonctionnelle et Evolutive (CEFE), Univ. Montpellier, CNRS, EPHE, IRD – Montpellier, France
3 ANTAGENE – La Tour de Salvagny, France
4 Fauna and Flora Service, Department of Territory and Sustainability – Barcelona, Spain
5 Medi Ambient, Conselh Generau d’Aran – Vielha, Spain
6 Departamento de Producción y Asistencias Técnicas, Sociedad Aragonesa de Gestión Agroambiental, S.L.U. – Huesca, Spain
7 Servicio de Biodiversidad, Sección de Espacios Naturales y Especies Amenazadas, Gobierno de Navarra-Nafarroako Gobernua – Pamplona-Iruñea, Spain
8 Unitat de Fauna, Departament de Medi Ambient – Andorra la Vella, Principality of Andorra
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
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     author = {Vanp\'e, C\'ecile and Pi\'edallu, Blaise and Quenette, Pierre-Yves and Sentilles, J\'er\^ome and Queney, Guillaume and Palaz\'on, Santiago and Jordana, Ivan Afonso and Jato, Ram\'on and Irurtia, Miguel Mari El\'osegui and de la Torre, Jordi Sol\`a and Gimenez, Olivier},
     title = {Estimating abundance of a recovering transboundary brown bear population with capture-recapture models},
     journal = {Peer Community Journal},
     eid = {e71},
     publisher = {Peer Community In},
     volume = {2},
     year = {2022},
     doi = {10.24072/pcjournal.199},
     url = {https://peercommunityjournal.org/articles/10.24072/pcjournal.199/}
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Vanpé, Cécile; Piédallu, Blaise; Quenette, Pierre-Yves; Sentilles, Jérôme; Queney, Guillaume; Palazón, Santiago; Jordana, Ivan Afonso; Jato, Ramón; Irurtia, Miguel Mari Elósegui; de la Torre, Jordi Solà; Gimenez, Olivier. Estimating abundance of a recovering transboundary brown bear population with capture-recapture models. Peer Community Journal, Volume 2 (2022), article  no. e71. doi : 10.24072/pcjournal.199. https://peercommunityjournal.org/articles/10.24072/pcjournal.199/

PCI peer reviews and recommendation, and links to data, scripts, code and supplementary information: 10.24072/pci.ecology.100103

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Balme, G. A.; Hunter, L. T. B.; Slotow, R. Evaluating Methods for Counting Cryptic Carnivores, Journal of Wildlife Management, Volume 73 (2009) no. 3, pp. 433-441 | DOI

[2] Bassi, C. Etude de la taille efficace et de la diversité génétique de la population d’ours brun, Ursus arctos, des Pyrénées, Rapport de stage de Master 2e année, Université d’Aix-Marseille, France, 2021

[3] Beaumelle, C. Evolution génétique et généalogie de la population des ours bruns (Ursus arctos) dans les Pyrénées, Rapport de stage de Master 1ere année, Université de Grenoble Alpes, France, 2016

[4] Bellemain, E.; Swenson, J. E.; Tallmon, D.; Brunberg, S.; Taberlet, P. Estimating Population Size of Elusive Animals with DNA from Hunter-Collected Feces: Four Methods for Brown Bears, Conservation Biology, Volume 19 (2005) no. 1, pp. 150-161 | DOI

[5] Berezowska-Cnota, T.; Luque-Márquez, I.; Elguero-Claramunt, I.; Bojarska, K.; Okarma, H.; Selva, N. Effectiveness of different types of hair traps for brown bear research and monitoring, PLOS ONE, Volume 12 (2017) no. 10 | DOI

[6] Bischof, R.; Brøseth, H.; Gimenez, O. Wildlife in a Politically Divided World: Insularism Inflates Estimates of Brown Bear Abundance, Conservation Letters, Volume 9 (2015) no. 2, pp. 122-130 | DOI

[7] Blanc, L.; Marboutin, E.; Gatti, S.; Gimenez, O. Abundance of rare and elusive species: Empirical investigation of closed versus spatially explicit capture-recapture models with lynx as a case study, The Journal of Wildlife Management, Volume 77 (2012) no. 2, pp. 372-378 | DOI

[8] Borchers, D.; Fewster, R. Spatial Capture–Recapture Models, Statistical Science, Volume 31 (2016) no. 2 | DOI

[9] Boulanger, J.; White, G.; McLellan, B.; Woods, J.; Proctor, M.; Himmer, S. A meta-analysis of grizzly bear DNA mark-recapture projects in British Columbia, Canada, Ursus, Volume 13 (2022), pp. 137-152 (https://www.jstor.org/stable/3873195)

[10] Bunnell, F.; Tait, D. Mortality Rates of North American Bears, ARCTIC, Volume 38 (1985) no. 4 | DOI

[11] Burnham, K.; Anderson, D. Model Selection and Multimodel Inference, Springer New York, New York, NY, 2004 | DOI

[12] Burton, A. C.; Neilson, E.; Moreira, D.; Ladle, A.; Steenweg, R.; Fisher, J. T.; Bayne, E.; Boutin, S. Wildlife camera trapping: a review and recommendations for linking surveys to ecological processes, Journal of Applied Ecology, Volume 52 (2015) no. 3, pp. 675-685 | DOI

[13] Camarra, J.; Sentilles, J.; Bombillon, N.; Gastineau, A.; Quenette, P. Suivi de l’ours brun dans les Pyrénées françaises (Sous-populations occidentale et centrale), Rapport annuel, Année 2015. Vincennes, France: Office National de la Chasse et de la Faune Sauvage , 2015 (https://docplayer.fr/43533649-Suivi-de-l-ours-brun-dans-les-pyrenees-francaises-sous-populations-occidentale-et-centrale-rapport-annuel-annee-2015.html)

[14] Castro-Arellano, I.; Madrid-Luna, C.; Lacher, T. E.; León-Paniagua, L. Hair-Trap Efficacy for Detecting Mammalian Carnivores in the Tropics, Journal of Wildlife Management, Volume 72 (2008) no. 6, pp. 1405-1412 | DOI

[15] Chapron, G.; Wielgus, R.; Quenette, P.-Y.; Camarra, J.-J. Diagnosing Mechanisms of Decline and Planning for Recovery of an Endangered Brown Bear (Ursus arctos) Population, PLoS ONE, Volume 4 (2009) no. 10 | DOI

[16] Creel, S.; Spong, G.; Sands, J. L.; Rotella, J.; Zeigle, J.; Joe, L.; Murphy, K. M.; Smith, D. Population size estimation in Yellowstone wolves with error‐prone noninvasive microsatellite genotypes, Molecular Ecology, Volume 12 (2003) no. 7, pp. 2003-2009 | DOI

[17] Cubaynes, S.; Pradel, R.; Choquet, R.; Duchamp, C.; Gaillard, J.-M.; Lebreton, J.-D.; Marboutin, E.; Miquel, C.; Reboulet, A.-M.; Poillot, C.; Taberlet, P.; Gimenez, O. Importance of Accounting for Detection Heterogeneity When Estimating Abundance: the Case of French Wolves, Conservation Biology, Volume 24 (2010) no. 2, pp. 621-626 | DOI

[18] Darimont, C. T.; Paquet, P. C.; Treves, A.; Artelle, K. A.; Chapron, G. Political populations of large carnivores, Conservation Biology, Volume 32 (2018) no. 3, pp. 747-749 | DOI

[19] De Barba, M.; Miquel, C.; Lobréaux, S.; Quenette, P. Y.; Swenson, J. E.; Taberlet, P. High-throughput microsatellite genotyping in ecology: improved accuracy, efficiency, standardization and success with low-quantity and degraded DNA, Molecular Ecology Resources, Volume 17 (2016) no. 3, pp. 492-507 | DOI

[20] De Barba, M.; Waits, L. P.; Garton, E. O.; Genovesi, P.; Randi, E.; Mustoni, A.; Groff, C. The power of genetic monitoring for studying demography, ecology and genetics of a reintroduced brown bear population, Molecular Ecology, Volume 19 (2010) no. 18, pp. 3938-3951 | DOI

[21] Dénes, F. V.; Silveira, L. F.; Beissinger, S. R. Estimating abundance of unmarked animal populations: accounting for imperfect detection and other sources of zero inflation, Methods in Ecology and Evolution, Volume 6 (2015) no. 5, pp. 543-556 | DOI

[22] Fagen, R.; Fagen, J. M. Individual Distinctiveness in Brown Bears, Ursus arctos L, Ethology, Volume 102 (2010) no. 2, pp. 212-226 | DOI

[23] Forney, K. A. Environmental Models of Cetacean Abundance: Reducing Uncertainty in Population Trends, Conservation Biology, Volume 14 (2000) no. 5, pp. 1271-1286 | DOI

[24] Forsyth, D. M.; Comte, S.; Davis, N. E.; Bengsen, A. J.; Côté, S. D.; Hewitt, D. G.; Morellet, N.; Mysterud, A. Methodology matters when estimating deer abundance: a global systematic review and recommendations for improvements, The Journal of Wildlife Management, Volume 86 (2022) no. 4 | DOI

[25] Frank, S. C.; Ordiz, A.; Gosselin, J.; Hertel, A.; Kindberg, J.; Leclerc, M.; Pelletier, F.; Steyaert, S. M. J. G.; Støen, O.-G.; Van de Walle, J.; Zedrosser, A.; Swenson, J. E. Indirect effects of bear hunting: a review from Scandinavia, Ursus, Volume 28 (2017) no. 2, pp. 150-164 | DOI

[26] Gavrilov, G.; Zlatanova, D.; Spasova, V.; Valchev, K.; Dutsov, A. Home range and habitat use of brown bear in Bulgaria: The first data based on GPS-telemetry, Acta Zool. Bulg., Volume 67 (2015), pp. 493-499

[27] Gervasi, V.; Br⊘seth, H.; Gimenez, O.; Nilsen, E. B.; Odden, J.; Flagstad, Ø.; Linnell, J. D. C. Sharing data improves monitoring of trans‐boundary populations: the case of wolverines in central Scandinavia, Wildlife Biology, Volume 22 (2016) no. 3, pp. 95-106 | DOI

[28] Gervasi, V.; Ciucci, P.; Davoli, F.; Boulanger, J.; Boitani, L.; Randi, E. Addressing challenges in non invasive capture-recapture based estimates of small populations: a pilot study on the Apennine brown bear, Conservation Genetics, Volume 11 (2010) no. 6, pp. 2299-2310 | DOI

[29] Gilpin, M.; Soulé, M. Minimum viable populations: processes of species extinction In: In Conservation biology: the science of scarcity and diversity:19-34. Soulé, M.E. (Ed.), Volume 4, Sinauer Associates, Sunderland, Massachusetts, USA (1986) no. 1, pp. 19-34 | DOI

[30] Gimenez, O. oliviergimenez/pyrenean-brown-bear-abundance: Pyrenean brown bear abundance (v1.0.0), Zenodo, 2022 | DOI

[31] González-Bernardo, E.; Bagnasco, C.; Bombieri, G.; Zarzo-Arias, A.; Ruiz-Villar, H.; Morales-González, A.; Lamamy, C.; Ordiz, A.; Cañedo, D.; Díaz, J.; Chamberlain, D. E.; Penteriani, V. Rubbing behavior of European brown bears: factors affecting rub tree selectivity and density, Journal of Mammalogy, Volume 102 (2021) no. 2, pp. 468-480 | DOI

[32] Halotel, Y. Analysis of brown bear, Ursus arctos, dispersal behaviour in the Pyrenees, Rapport de stage de Master 2e année, Université de Montpellier, France, 2022

[33] Henle, K.; Gruber, B. Performance of multistate mark–recapture models for temporary emigration in the presence of survival costs, Methods in Ecology and Evolution, Volume 9 (2017) no. 3, pp. 657-667 | DOI

[34] Huber, D.; Roth, H. U. Movements of European brown bears in Croatia, Acta Theriologica, Volume 38 (1993), pp. 151-159 | DOI

[35] Keating, K.; Schwartz, C.; Haroldson, M.; Moody, D. Estimating numbers of females with cubs-of-the-year in the Yellowstone grizzly bear population, Ursus, Volume 13 (2002), pp. 161-174 (https://www.jstor.org/stable/3873197)

[36] Kendall, K.; McKelvey, K. Hair collection In: In Noninvasive survey methods for North American carnivores Long, R.A., MacKay, P., Ray, J.C. & Zielinski, W.J. (Eds.). , Island Press, Washington, DC (2008), pp. 35-176 (https://islandpress.org/books/noninvasive-survey-methods-carnivores)

[37] Kendall, W. L.; Nichols, J. D.; Hines, J. E. Estimating Temporary Emigration Using Capture-Recapture Data with Pollock's Robust Design, Ecology, Volume 78 (1997) no. 2 | DOI

[38] Kendall, W. L.; Pollock, K. H.; Brownie, C. A Likelihood-Based Approach to Capture-Recapture Estimation of Demographic Parameters under the Robust Design, Biometrics, Volume 51 (1995) no. 1 | DOI

[39] Laake, J. RMark: An R interface for analysis of capture-recapture data with MARK, AFSC Processed Rep. 2013-01, 25 p. Alaska Fish. Sci. Cent., NOAA, Natl. Mar. Fish. Serv., 7600 Sand Point Way NE, Seattle WA 98115, 2013 (https://repository.library.noaa.gov/view/noaa/4372)

[40] Lampa, S.; Henle, K.; Klenke, R.; Hoehn, M.; Gruber, B. How to overcome genotyping errors in non-invasive genetic mark-recapture population size estimation-A review of available methods illustrated by a case study, The Journal of Wildlife Management, Volume 77 (2013) no. 8, pp. 1490-1511 | DOI

[41] Le Maho, Y.; Boitani, L.; Clobert, J.; Quenette, P.; Sarrazin, F.; Savouré-Soubelet, A. Expertise collective scientifique « L’Ours brun dans les Pyrénées », Paris, France: Muséum National d’Histoire Naturelle, 2013 (https://lciepub.nina.no/pdf/635379157217795378_2013-09-26-Expertise-Collective-Scientifique-Ours-Pyrenees-Museum-National-Histoire-Naturelle-MNHN.pdf)

[42] Spínola, M. Noninvasive Survey Methods for Carnivores, Journal of Wildlife Management, Volume 73 (2009) no. 8, p. 1445-1445 | DOI

[43] Lukacs, P. Statistical aspects of using genetic markers for individual identification in capture-recapture studies, Ph.D. thesis, Colorado State University, USA (2005) (https://www.researchgate.net/publication/265931941_Statistical_aspects_of_using_genetic_markers_for_individual_identification_in_capture-recapture_studies)

[44] Lukacs, P. M.; Burnham, K. P. Review of capture-recapture methods applicable to noninvasive genetic sampling, Molecular Ecology, Volume 14 (2005) no. 13, pp. 3909-3919 | DOI

[45] Martin, J.; Revilla, E.; Quenette, P.-Y.; Naves, J.; Allainé, D.; Swenson, J. E. Brown bear habitat suitability in the Pyrenees: transferability across sites and linking scales to make the most of scarce data, Journal of Applied Ecology, Volume 49 (2012), pp. 621-631 | DOI

[46] McCall, B. S.; Mitchell, M. S.; Schwartz, M. K.; Hayden, J.; Cushman, S. A.; Zager, P.; Kasworm, W. F. Combined use of mark-recapture and genetic analyses reveals response of a black bear population to changes in food productivity, The Journal of Wildlife Management, Volume 77 (2013) no. 8, pp. 1572-1582 | DOI

[47] McGowan, C. P.; Runge, M. C.; Larson, M. A. Incorporating parametric uncertainty into population viability analysis models, Biological Conservation, Volume 144 (2011) no. 5, pp. 1400-1408 | DOI

[48] McLellan, B. N. Some mechanisms underlying variation in vital rates of grizzly bears on a multiple use landscape, The Journal of Wildlife Management, Volume 79 (2015) no. 5, pp. 749-765 | DOI

[49] Mcloughlin, P. D.; Ferguson, S. H.; Messier, F. Intraspecific Variation in Home Range Overlap with Habitat Quality: A Comparison among Brown Bear Populations, Evolutionary Ecology, Volume 14 (2000) no. 1, pp. 39-60 | DOI

[50] Mertzanis, Y.; Ioannis, I.; Mavridis, A.; Nikolaou, O.; Riegler, S.; Riegler, A.; Tragos, A. Movements, activity patterns and home range of a female brown bear (Ursus arctos, L.) in the Rodopi Mountain Range, Greece, Belgian J. Zool., Volume 135 (2005), pp. 217-221

[51] Miotto, R. A.; Rodrigues, F. P.; Ciocheti, G.; Galetti, P. M. Determination of the Minimum Population Size of Pumas (Puma concolor) Through Fecal DNA Analysis in Two Protected Cerrado Areas in the Brazilian Southeast, Biotropica, Volume 39 (2007) no. 5, pp. 647-654 | DOI

[52] Miquel, C.; Bellemain, E.; Poillot, C.; Bessière, J.; Durand, A.; Taberlet, P. Quality indexes to assess the reliability of genotypes in studies using noninvasive sampling and multiple-tube approach, Molecular Ecology Notes, Volume 6 (2006) no. 4, pp. 985-988 | DOI

[53] Morin, D. J.; Boulanger, J.; Bischof, R.; Lee, D. C.; Ngoprasert, D.; Fuller, A. K.; McLellan, B.; Steinmetz, R.; Sharma, S.; Garshelis, D.; Gopalaswamy, A.; Nawaz, M. A.; Karanth, U. Comparison of methods for estimating density and population trends for low-density Asian bears, Global Ecology and Conservation, Volume 35 (2022) | DOI

[54] Mowat, G.; Strobeck, C. Estimating Population Size of Grizzly Bears Using Hair Capture, DNA Profiling, and Mark-Recapture Analysis, The Journal of Wildlife Management, Volume 64 (2000) no. 1 | DOI

[55] Murray, D.; Sandercock, B. Population ecology in practice, John Wiley & Sons, 2020 (https://www.wiley.com/en-us/Population+Ecology+in+Practice-p-9780470674147)

[56] Nichols, J.; Williams, B. Monitoring for conservation, Trends in Ecology & Evolution, Volume 21 (2006) no. 12, pp. 668-673 | DOI

[57] Otis, D.; Burnham, K.; White, G.; Anderson, D. Statistical inference from capture data on closed animal populations, Wild. Monogr. , Volume 62 (1978), pp. 3-135 (https://pubs.er.usgs.gov/publication/70119899)

[58] Parres, A.; Palazón, S.; Afonso, I.; Quenette, P.-Y.; Batet, A.; Camarra, J.-J.; Garreta, X.; Gonçalves, S.; Guillén, J.; Mir, S.; Jato, R.; Rodríguez, J.; Sentilles, J.; Xicola, L.; Melero, Y. Activity patterns in the reintroduced Pyrenean brown bear population, Mammal Research, Volume 65 (2020) no. 3, pp. 435-444 | DOI

[59] Pederson, J. C.; Bunnell, K. D.; Conner, M. M.; McLaughlin, C. R. A robust-design analysis to estimate American black bear population parameters in Utah, Ursus, Volume 23 (2012) no. 1, pp. 104-116 | DOI

[60] Petit, E.; Valiere, N. Contributed Papers: Estimating Population Size with Noninvasive Capture-Mark-Recapture Data, Conservation Biology, Volume 20 (2006) no. 4, pp. 1062-1073 | DOI

[61] Piel, A. K.; Crunchant, A.; Knot, I. E.; Chalmers, C.; Fergus, P.; Mulero-Pázmány, M.; Wich, S. A. Noninvasive Technologies for Primate Conservation in the 21st Century, International Journal of Primatology, Volume 43 (2021) no. 1, pp. 133-167 | DOI

[62] Plummer, M. JAGS: A program for analysis of Bayesian graphical models using Gibbs sampling In: In Proceedings of the 3rd international workshop on distributed statistical computing. Hornik, K., Leisch, F. & Zeileis, A. (Eds.). Vol. 124, No. 125. 10. Vienna, Austria (2003) (http://hdl.handle.net/20.500.12708/22149)

[63] Pollock, K. H. A Capture-Recapture Design Robust to Unequal Probability of Capture, The Journal of Wildlife Management, Volume 46 (1982) no. 3 | DOI

[64] Proctor, M. F.; Garshelis, D. L.; Thatte, P.; Steinmetz, R.; Crudge, B.; McLellan, B. N.; McShea, W. J.; Ngoprasert, D.; Nawaz, M. A.; Te Wong, S.; Sharma, S.; Fuller, A. K.; Dharaiya, N.; Pigeon, K. E.; Fredriksson, G.; Wang, D.; Li, S.; Hwang, M.-h. Review of field methods for monitoring Asian bears, Global Ecology and Conservation, Volume 35 (2022) | DOI

[65] Quenette, P.; Jonozovic, M.; Marinsic, A.; Camarra, J.; Guinot-Ghestem, M.; Sentilles, J.; Steinmetzn J.; Vanpé, C.; lban, N. First translocation of females in the French Western Pyrenees: a new step in the long process of brown bear restoration in the Pyrenees Mountains, Bear News, Volume 28 (2019), pp. 11-13 (https://www.researchgate.net/publication/335450744_First_translocation_of_females_in_the_French_Western_Pyrenees_a_new_step_in_the_long_process_of_brown_bear_restoration_in_the_Pyrenees_Mountains)

[66] Quinn, T. P.; Wirsing, A. J.; Proctor, M. Optimal barbed wire height for brown bear hair sample collection, Ursus, Volume 2022 (2022) no. 33e2 | DOI

[67] Rankin, R. W.; Nicholson, K. E.; Allen, S. J.; Krützen, M.; Bejder, L.; Pollock, K. H. A Full-Capture Hierarchical Bayesian Model of Pollock's Closed Robust Design and Application to Dolphins, Frontiers in Marine Science, Volume 3 (2016) | DOI

[68] RCoreTeam R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing, Vienna, Austria, 2013 (https://www.R-project.org/)

[69] Riecke, T. V.; Leach, A. G.; Gibson, D.; Sedinger, J. S. Parameterizing the robust design in the BUGS language: Lifetime carry‐over effects of environmental conditions during growth on a long‐lived bird, Methods in Ecology and Evolution, Volume 9 (2018) no. 11, pp. 2294-2305 | DOI

[70] Royle, J.; Chandler, R. B.; Sollmann, R.; Gardner, B. Fully Spatial Capture-Recapture Models, Spatial Capture-recapture, Elsevier, 2014, pp. 125-170 | DOI

[71] Schofield, M. R.; Barker, R. J. Full Open Population Capture–Recapture Models With Individual Covariates, Journal of Agricultural, Biological, and Environmental Statistics, Volume 16 (2011) no. 2, pp. 253-268 | DOI

[72] Sentilles, J.; Lemaître, P.; Vanpé, C.; Quenette, P. Rapport annuel du réseau ours brun 2021, Paris, France: Office Français de la Biodiversité, 2022 (https://professionnels.ofb.fr/fr/doc/ours-infos-2021)

[73] Sentilles, J.; Vanpé, C.; Quenette, P.-Y. Benefits of incorporating a scat-detection dog into wildlife monitoring: a case study of Pyrenean brown bear, Journal of Vertebrate Biology, Volume 69 (2021) no. 3 | DOI

[74] Solberg, K. H.; Bellemain, E.; Drageset, O.-M.; Taberlet, P.; Swenson, J. E. An evaluation of field and non-invasive genetic methods to estimate brown bear (Ursus arctos) population size, Biological Conservation, Volume 128 (2006) no. 2, pp. 158-168 | DOI

[75] Spady, T. J.; Lindburg, D. G.; Durrant, B. S. Evolution of reproductive seasonality in bears, Mammal Review, Volume 37 (2007) no. 1, pp. 21-53 | DOI

[76] Staton, B. A.; Justice, C.; White, S.; Sedell, E. R.; Burns, L. A.; Kaylor, M. J. Accounting for uncertainty when estimating drivers of imperfect detection: An integrated approach illustrated with snorkel surveys for riverine fishes, Fisheries Research, Volume 249 (2022) | DOI

[77] Stetz, J. B.; Kendall, K. C.; Servheen, C. Evaluation of Bear Rub Surveys to Monitor Grizzly Bear Population Trends, Journal of Wildlife Management, Volume 74 (2010) no. 4, pp. 860-870 | DOI

[78] Swenson, J.; Sandegren, F.; Brunberg, S.; Segerström, P.; Segerstrøm, P. Factors associated with loss of brown bear cubs in Sweden, Ursus, Volume 12 (2001), pp. 69-80 (https://www.bearbiology.org/wp-content/uploads/2017/10/Swenson_Sandegren_Vol_12.pdf)

[79] Swenson, J. E.; Sandegren, F.; Söderberg, A.; Bjärvall, A.; Franzén, R.; Wabakken, P. Infanticide caused by hunting of male bears, Nature, Volume 386 (1997) no. 6624, pp. 450-451 | DOI

[80] Taberlet, P.; Camarra, J.-J.; Griffin, S.; Uhres, E.; Hanotte, O.; Waits, L. P.; Dubois-Paganon, C.; Burke, T.; Bouvet, J. Noninvasive genetic tracking of the endangered Pyrenean brown bear population, Molecular Ecology, Volume 6 (1997) no. 9, pp. 869-876 | DOI

[81] Taberlet, P. Reliable genotyping of samples with very low DNA quantities using PCR, Nucleic Acids Research, Volume 24 (1996) no. 16, pp. 3189-3194 | DOI

[82] Thompson, W. Sampling rare or elusive species: concepts, designs, and techniques for estimating population parameters, Island Press, Washington, D.C., USA, 2013

[83] Tosoni, E.; Boitani, L.; Gentile, L.; Gervasi, V.; Latini, R.; Ciucci, P. Assessment of key reproductive traits in the Apennine brown bear population, Ursus, Volume 28 (2017) no. 1 | DOI

[84] Tourani, M. A review of spatial capture–recapture: Ecological insights, limitations, and prospects, Ecology and Evolution, Volume 12 (2021) no. 1 | DOI

[85] UICN France, M. S. &. O. La Liste rouge des espèces menacées en France – Chapitre Mammifères de France métropolitaine, Paris, France, 2017 (https://uicn.fr/liste-rouge-mammiferes/)

[86] Vanpé, C.; Sentilles, J.; Lemaître, P.; Desbarax, R.; Bibal, D.; Darmani, G.; Labal, P.; Quenette, P. Cartographie quinquennale (2016-2020) de l’aire de répartition de l’ours brun dans les Pyrénées françaises, Vincennes, France: Office Français de la Biodiversité, 2021 | DOI

[87] Waits, L. P.; Paetkau, D. Noninvasive genetic sampling tools for wildlife biologists: a review of applications and recommendations for accurate data collection, Journal of Wildlife Management, Volume 69 (2005) no. 4, pp. 1419-1433 | DOI

[88] White, G. C.; Burnham, K. P. Program MARK: survival estimation from populations of marked animals, Bird Study, Volume 46 (1999) no. sup1 | DOI

[89] Williams, B.; Nichols, J.; Conroy, M. Analysis and management of animal populations, Academic press, 2002 (https://www.elsevier.com/books/analysis-and-management-of-animal-populations/williams/978-0-12-754406-9)

[90] Wilson, G. J.; Delahay, R. J. A review of methods to estimate the abundance of terrestrial carnivores using field signs and observation, Wildlife Research, Volume 28 (2001) no. 2 | DOI

[91] Woods, J.; Paetkau, D.; Lewis, D.; McLellan, B.; Proctor, M.; Strobeck, C. Genetic tagging of free-ranging black and brown bears, Wildl. Soc. Bull. , Volume 27 (1999), pp. 616-627 (https://www.jstor.org/stable/3784082)

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