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Reliability of multinomial N-mixture models for estimating abundance of small terrestrial vertebrates

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Abstract

Information on population abundance is important to correctly plan conservation and management of animal populations. In general, capture-mark-recapture (CMR) is considered the most robust technique to estimate population abundance, but it is costly in terms of time and effort. Recently, binomial N-mixture models, based on counts of unmarked individuals, have been widely employed to estimate abundance. These models have limits and their reliability has been criticized. In the majority of cases, multinomial N-mixture models based on multiple observer protocols, that are hierarchical extensions of simple CMR, are applied in estimating abundance of animals with large body size, conspicuous behavior or high detection probabilities. We applied and evaluated the reliability of a multinomial N-mixture modelling approach with multiple observer data to a small and cryptic terrestrial salamander, found in different habitats where populations possess different level of detectability. Estimates obtained with multinomial N-mixture models were compared to estimates obtained with classical methods, such as removal sampling, and their reliability has also been evaluated by simulations scenarios. Our results show that multinomial N-mixture models, applied within a multiple observer framework, give reliable and robust estimates of population abundance even when detection and density are relatively low. Therefore, multinomial N-mixture models appear efficient and cost-effective when planning and identifying management actions and conservation programs of small terrestrial animals such as amphibians and reptiles.

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References

  • Ariefiandy A, Purwandana D, Seno A, Chrismiawati M, Ciofi C, Jessop TS (2014) Evaluation of three field monitoring-density estimation protocols and their relevance to Komodo dragon conservation. Biodivers Conserv 23:2473–2490

    Google Scholar 

  • Barker RJ, Schofield MR, Link WA, Sauer JR (2017) On the reliability of N-Mixture models for count data. Biometrics 74:369–377

    PubMed  Google Scholar 

  • Blondel J, Aronson J (1999) Biology and wildlife of the Mediterranean region. Oxford University Press, Oxford

    Google Scholar 

  • Borchers DL, Buckland ST, Stephens WE, Zucchini W (2002) Estimating animal abundance. Springer, London, UK

    Google Scholar 

  • Bröker KCA, Hansen RG, Leonard KE, Koski WR, Heide-Jørgensen MP (2019) A comparison of image and observer based aerial surveys of narwhal. Mar Mam Sci 35:1253–1279

    Google Scholar 

  • Bruce RC (1995) The use of temporary removal sampling in a study of population dynamics of the salamander Desmognathus monticola. Austral Ecol 20:403–412

    Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection multimodel inference a practical information-theoretic approach. Springer, New York

    Google Scholar 

  • Chandler RB, Royle JA, King DI (2011) Inference about density and temporary emigration in unmarked populations. Ecology 92:1429–1435

    PubMed  Google Scholar 

  • Cook RD, Jacobson JO (1979) A design for estimating visibility bias in aerial surveys. Biometrics 35:735–742

    Google Scholar 

  • Costa A, Crovetto F, Salvidio S (2016) European plethodontid salamanders on the forest floor: local abundance is related to fine-scale environmental factors. Herpetol Conserv Biol 11:344–349

    Google Scholar 

  • Costa A, Oneto F, Salvidio S (2019) Time-for-space substitution in N-mixture modeling and population monitoring. J Wildlife Manage 83:737–741

    Google Scholar 

  • Duarte A, Adams MJ, Peterson JT (2018) Fitting N-mixture models to count data with unmodeled heterogeneity: Bias, diagnostics, and alternative approaches. Ecol modell 374:51–59

    Google Scholar 

  • Ficetola GF, Barzaghi B, Melotto A, Muraro M, Lunghi E, Canedoli C, Carretero MA (2018) N-mixture models reliably estimate the abundance of small vertebrates. Sci Rep 8:10357

    PubMed  PubMed Central  Google Scholar 

  • Fiske I, Chandler R (2011) Unmarked: an R package for fitting hierarchical models of wildlife occurrence and abundance. J Stat Softw 43:1–23

    Google Scholar 

  • Grant EHC, Jung RE, Nichols JD, Hines JE (2005) Double-observer approach to estimating egg mass abundance of pool-breeding amphibians. Wetl Ecol Manag 13:305–320

    Google Scholar 

  • Griffiths RA, Foster J, Wilkinson JW, Sewell D (2015) Science, statistics and surveys: a herpetological perspective. J Appl Ecol 52:1413–1417

    PubMed  PubMed Central  Google Scholar 

  • Hone J (2008) On bias, precision and accuracy in wildlife aerial surveys. Wildl Res 35:253–257

    Google Scholar 

  • Jiménez J, Moreno-Opo R, Carrasco M, Feliu J (2015) Estimating the abundance and habitat selection of conservation priority marsh-dwelling passerines with a double-observer approach. Ardeola 62:269–281

    Google Scholar 

  • Jung RE, Royle JA, Sauer JR, Addison C, Rau RD, Shirk JL, Whissel JC (2005) Estimation of stream salamander (Plethodontidae, Desmognathinae and Plethodontinae) populations in Shenandoah National Park, Virginia, USA. Alytes 22:72–84

    Google Scholar 

  • Kéry M (2018) Identifiability in N-mixture models: a large-scale screening test with bird data. Ecology 99:281–288

    PubMed  Google Scholar 

  • Kéry M, Royle JA (2016) Applied hierarchical modelling in ecology. Academic Press, Cambridge

    Google Scholar 

  • Knape J, Arlt D, Barraquand F, Berg Å, Chevalier M, Pärt T, Ruete A, Żmihorski M (2018) Sensitivity of binomial N-mixture models to overdispersion: the importance of assessing model fit. Methods Ecol Evol 9:2102–2114

    Google Scholar 

  • Koneff MD, Royle JA, Otto MC, Wortham JS, Bidwell JK (2008) A double-observer method to estimate detection rate during aerial waterfowl surveys. J Wildlife Manage 72:1641–1649

    Google Scholar 

  • Langtimm CA, Dorazio RM, Stith BM, Doyle TJ (2011) New aerial survey and hierarchical model to estimate manatee abundance. J Wildlife Manage 75:399–412

    Google Scholar 

  • Lanza B (2007) Speleomantes strinatii (Aellen). In: Lanza B, Andreone F, Bologna MA, Corti C, Razzetti E (eds) Fauna d’Italia—Amphibia. Edizioni Calderini, Bologna, pp 152–156

    Google Scholar 

  • Leston L, Koper N, Rosa P (2015) Perceptibility of prairie songbirds using double-observer point counts. Great Plains Res. 25:53–61

    Google Scholar 

  • Lincoln FC (1930). Calculating waterfowl abundance on the basis of banding returns. U.S. Department of Agriculture, Circular 118, Washington DC

  • Lindstrom L, Reeve R, Salvidio S (2010) Bayesian salamanders: analysing the demography of an underground population of the European plethodontid Speleomantes strinatii with state-space modelling. BMC Ecol 10:4

    PubMed  PubMed Central  Google Scholar 

  • Link WA, Schofield MR, Barker RJ, Sauer JR (2018) On the robustness of N-mixture models. Ecology 99:1547–1551

    PubMed  Google Scholar 

  • MacKenzie DI, Bailey LL (2004) Assessing the fit of site-occupancy models. J Agric Biol Environ Stat 9:300–318

    Google Scholar 

  • McDiarmid RW, Foster MS, Guyer C, Gibbons JW, Chernoff N (2012) Reptile biodiversity. Standard methods for inventorying and monitoring. University of California Press, Berkeley

    Google Scholar 

  • Nichols JD, Conroy MJ (1996) Techniques for estimating abundance and species richness. In: Wilson DE, Russel CF, Nichols JD, Rudram R, Foster MS (eds) Measuring and monitoring biological diversity—standard methods for mammals. Smithsonian Institution Press, Washington and London, pp 177–179

    Google Scholar 

  • Nichols JD, Hines JE, Sauer JR, Fallon F, Fallon J, Heglund PJ (2000) A double-observer approach for estimating detection probability and abundance from avian point counts. Auk 117:393–408

    Google Scholar 

  • Petranka JW, Murray SS (2001) Effectiveness of removal sampling for determining salamander density and biomass: a case study in an Appalachian streamside community. J Herpetol 35:36–44

    Google Scholar 

  • Priol P, Mazerolle MJ, Imbeau L, Drapeau P, Trudeau C, Ramiere J (2014) Using dynamic N-mixture models to test cavity limitation on northern flying squirrel demographic parameters using experimental nest box supplementation. Ecol Evol 4:2165–2177

    PubMed  PubMed Central  Google Scholar 

  • Romano A, Costa A, Basile M, Raimondi R, Posillico M, Scinti Roger D, Crisci A, Piraccini R, Raia P, Matteucci G, De Cinti B (2017) Conservation of salamanders in managed forests: Methods and costs of monitoring abundance and habitat selection. Forest Ecol Manag 400:12–18

    Google Scholar 

  • Royle JA (2004a) Generalized estimators of avian abundance from spatially replicated count survey data. Anim Biodivers Conserv 27:375–386

    Google Scholar 

  • Royle JA (2004b) N-mixture models for estimating population size from spatially replicated counts. Biometrics 60:108–115

    PubMed  Google Scholar 

  • Royle JA, Dorazio RM (2006) Hierarchical models of animal abundance and occurrence. J Agric Biol Environ Stat 11:249–263

    Google Scholar 

  • Salvidio S (2001) Estimating terrestrial salamander abundance in different habitats: efficiency of temporary removal methods. Herpetol Rev 32:21–24

    Google Scholar 

  • Salvidio S (2007) Population dynamics and regulation in the cave salamander Speleomantes strinatii. Naturwissenschaften 94:396–400

    CAS  PubMed  Google Scholar 

  • Salvidio S, Lattes A, Tavano M, Melodia F, Pastorino MV (1994) Ecology of a Speleomantes ambrosii population inhabiting an artificial tunnel. Amphibia-Reptilia 15:35–45

    Google Scholar 

  • Salvidio S, Oneto F, Ottonello D, Pastorino MV (2016) Lagged influence of North Atlantic Oscillation on population dynamics of a Mediterranean terrestrial salamander. Int J Biometeorol 60:475–480

    PubMed  Google Scholar 

  • Salvidio S, Romano A, Palumbi G, Costa A (2017) Safe caves and dangerous forests? Predation risk may contribute to salamander colonization of subterranean habitats. Sci Nat 104:20

    Google Scholar 

  • Schmidt BR (2003) Count data, detection probabilities, and the demography, dynamics, distribution, and decline of amphibians. CR Biol 326:S119–S124

    Google Scholar 

  • Seber GAF (1982) Estimating animal abundance and related parameters, 2nd edn. Charles Griffin and Co., London

    Google Scholar 

  • Southwell C (1996) Estimation of population size and density when counts are incomplete. In: Wilson DE, Russel CF, Nichols JD, Rudram R, Foster MS (eds) Measuring and monitoring biological diversity—standard methods for mammals. Smithsonian Institution Press, Washington and London, pp 196–210

    Google Scholar 

  • Specht HM, Reich HT, Iannarilli F, Edwards MR, Stapleton SP, Weegman MD, Arnold TW (2017) Occupancy surveys with conditional replicates: an alternative sampling design for rare species. Methods Ecol Evol 8:1725–1734

    Google Scholar 

  • Veech JA, Ott JR, Troy JR (2016) Intrinsic heterogeneity in detection probability and its effect on N-mixture models. Methods Ecol Evol 7:1019–1028

    Google Scholar 

  • Vrtiska MP, Powell LA (2011) estimates of duck breeding populations in the nebraska sandhills using double observer methodology. Waterbirds 34:96–101

    Google Scholar 

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

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

    Google Scholar 

  • Yoccoz NG, Nichols JD, Boulinier T (2001) Monitoring of biological diversity in space and time. Trends Ecol Evol 16:446–453

    Google Scholar 

Download references

Acknowledgements

The authors declare that this study did not receive any funding, nor there is any competing financial interest, that could have altered its outcome. Permits for salamander capture and temporary removal were issued by the Italian Ministry of Environment (# 2426 of 25/02/2019). We are grateful to three anonymous reviewers for their valuable comments on a previous version of the study.

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Correspondence to Andrea Costa.

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Communicated by Clinton Jenkins.

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Costa, A., Romano, A. & Salvidio, S. Reliability of multinomial N-mixture models for estimating abundance of small terrestrial vertebrates. Biodivers Conserv 29, 2951–2965 (2020). https://doi.org/10.1007/s10531-020-02006-5

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