Skip to main content Accessibility help
×
Home

Counting Sunda clouded leopards with confidence: incorporating individual heterogeneity in density estimates

  • Azlan Mohamed (a1), Rahel Sollmann (a2), Seth Timothy Wong (a1), Jürgen Niedballa (a1), Jesse F. Abrams (a1), Johnny Kissing (a3) and Andreas Wilting (a1)...

Abstract

Even with intensive sampling effort, data often remain sparse when estimating population density of elusive species such as the Sunda clouded leopard Neofelis diardi. An inadequate number of recaptures can make it difficult to account for heterogeneity in detection parameters. We used data from large-scale camera-trapping surveys in three forest reserves in Sabah, Malaysian Borneo, to (1) examine whether a high-density camera-trap network increases the number of recaptures for females, which tend to be more difficult to detect, thus improving the accuracy of density estimates; (2) compare density estimates from models incorporating individual heterogeneity in detection parameters with estimates from the null model to evaluate its potential bias; and (3) investigate how the size of the camera-trap grid affects density and movement estimates. We found that individual heterogeneity could not be incorporated in the single-site data analysis and only conservative null model estimates could be generated. However, aggregating data across study sites enabled us to account for individual heterogeneity and we estimated densities of 1.27–2.82 individuals/100 km2, 2–3 times higher than estimates from null models. In light of these findings, it is possible that earlier studies underestimated population density. Similar densities found in well-managed forest and recently selectively logged forest suggest that Sunda clouded leopards are relatively resilient to forest disturbances. Our analysis also revealed that camera-trapping grids for Sunda clouded leopard density estimations should cover large areas (c. 250 km2), although smaller grids could be appropriate if density or detectability are higher.

Copyright

Corresponding author

(Corresponding author) E-mail azlan.mohamed@gmail.com

Footnotes

Hide All
*

Also at: WWF-Malaysia, Petaling Jaya, Selangor, Malaysia

Supplementary material for this article is available at https://doi.org/10.1017/S0030605318001503

Footnotes

References

Hide All
Borchers, D.L. & Efford, M.G. (2008) Spatially explicit maximum likelihood methods for capture–recapture studies. Biometrics, 64, 377385.
Bowler, M.T., Tobler, M.W., Endress, B.A., Gilmore, M.P. & Anderson, M.J. (2016) Estimating mammalian species richness and occupancy in tropical forest canopies with arboreal camera traps. Remote Sensing in Ecology and Conservation, 3, 146157.
Brodie, J.F. & Giordano, A.J. (2012) Density of the Vulnerable Sunda clouded leopard Neofelis diardi in a protected area in Sabah, Malaysian Borneo. Oryx, 46, 427430.
Cheyne, S.M., Stark, D.J., Limin, S.H. & Macdonald, D.W. (2013) First estimates of population ecology and threats to Sunda clouded leopards Neofelis diardi in a peat-swamp forest, Indonesia. Endangered Species Research, 22, 19.
Cubaynes, S., Pradel, R., Choquet, R., Duchamp, C., Gaillard, J.M., Lebreton, J.D. et al. (2010) Importance of accounting for detection heterogeneity when estimating abundance: the case of French wolves. Conservation Biology, 24, 621626.
Dillon, A. & Kelly, M.J. (2008) Ocelot home range, overlap and density: comparing radio telemetry with camera trapping. Journal of Zoology, 275, 391398.
Efford, M.G. (2016) Spatially explicit capture recapture. R package version 2.10.4. http://cran.r-project.org/web/package/secr/index.html [accessed 7 January 2017].
Efford, M.G. & Fewster, R.M. (2013) Estimating population size by spatially explicit capture–recapture. Oikos, 122, 918928.
Efford, M.G., Borchers, D.L. & Byrom, A.E. (2009) Density estimation by spatially explicit capture–recapture: likelihood-based methods. In Modeling Demographic Processes in Marked Populations (eds Thomson, D.L., Cooch, E.G. & Conroy, M.J.), pp. 255269. Springer, New York, USA.
Gaveau, D.L.A., Wandono, H. & Setiabudi, F. (2007) Three decades of deforestation in southwest Sumatra: have protected areas halted forest loss and logging, and promoted re-growth? Biological Conservation, 4, 495504.
Gaveau, D.L.A., Sheil, D., Husnayaen, , Salim, M.A., Arjasakusuma, S., Ancrenaz, M. et al. (2016) Rapid conversions and avoided deforestation: examining four decades of industrial plantation expansion in Borneo. Scientific Reports, 6, 32017.
Hearn, A., Sanderson, J., Ross, J., Wilting, A. & Sunarto, S. (2008) Neofelis diardi ssp. borneensis. In The IUCN Red List of Threatened Species 2008: e.T136945A4351615. http://dx.doi.org/10.2305/IUCN.UK.2008.RLTS.T136945A4351615.en [accessed 15 July 2017].
Hearn, A.J., Ross, J., Pamin, D., Bernard, H., Hunter, L. & Macdonald, D.W. (2013) Insights into the spatial and temporal ecology of the Sunda clouded leopard Neofelis diardi. Raffles Bulletin of Zoology, 61, 871875.
Hearn, A., Ross, J., Brodie, J., Cheyne, S., Haidir, I.A., Loken, B. et al. (2015) Neofelis diardi. In The IUCN Red List of Threatened Species 2015: e.T136603A97212874. http://dx.doi.org/10.2305/IUCN.UK.2015-4.RLTS.T136603A50664601.en [accessed 15 July 2017].
Hearn, A.J., Ross, J., Macdonald, D.W., Bolongon, G., Cheyne, S.M., Mohamed, A. et al. (2016) Predicted distribution of the Sunda clouded leopard Neofelis diardi (Mammalia: Carnivora: Felidae) on Borneo. Raffles Bulletin of Zoology, Supplement No. 33, 149156.
Hearn, A.J., Ross, J., Bernard, H., Bakar, S.A., Goossens, B., Hunter, L.T.B. & Macdonald, D.W. (2017) Responses of Sunda clouded leopard Neofelis diardi population density to anthropogenic disturbance: refining estimates of its conservation status in Sabah. Oryx, published online 27 September 2017.
Howe, E.J., Obbard, M.E. & Kyle, C.J. (2013) Combining data from 43 standardized surveys to estimate densities of female American black bears by spatially explicit capture–recapture. Population Ecology, 55, 595607.
Jenny, D. (1996) Spatial organization of leopards Panthera pardus in Tai National Park, Ivory Coast: is rainforest habitat a ‘tropical haven’? Journal of Zoology, 240, 427440.
Karanth, K.U. & Sunquist, M.E. (2000) Behavioural correlates of predation by tiger (Panthera tigris), leopard (Panthera pardus), and dhole (Cuon alpinus) in Nagarahole, India. Journal of Zoology, 250, 255265.
Karanth, K.U., Nichols, J.D., Kumar, N.S. & Hines, J.D. (2006) Assessing tiger population dynamics using photographic capture–recapture sampling. Ecology, 87, 29252937.
Kleinschroth, F. & Healey, J.R. (2017) Impacts of logging roads on tropical forests. Biotropica, 49, 620635.
Lagan, P., Mannan, S. & Matsubayashi, H. (2007) Sustainable use of tropical forests by reduced-impact logging. Ecological Research, 22, 414421.
Larrucea, E.S., Brussard, P.F., Jaeger, M.M. & Barrett, R.H. (2006) Cameras, coyotes, and the assumption of equal detectability. Journal of Wildlife Management, 71, 16821689.
Mohamad, S.W., Rayan, D.M., Christopher, W.C.T., Hamirul, M., Mohamed, A., Lau, C.F. & Siwan, E.S. (2015) The first description of population density and habitat use of the mainland clouded leopard Neofelis nebulosa within a logged primary forest in South East Asia. Population Ecology, 57, 495503.
Niedballa, J., Sollmann, R., Courtiol, A. & Wilting, A. (2016) CamtrapR: an R package for efficient camera trap data management. Methods in Ecology and Evolution, 7, 14571462.
Otis, D.L., Burnham, K.P., White, G.C. & Anderson, D.R. (1978) Statistical Inference from Capture Data on Closed Animal Populations. Wildlife Monographs Series, no. 62. The Wildlife Society, Bethesda, USA.
Pledger, S. (2000) Unified maximum likelihood estimates for closed capture–recapture models using mixture. Biometrics, 56, 434442.
R Core Team (2017) R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
Singh, R., Qureshi, Q., Sankar, K., Krausman, P.R. & Goyal, S.P. (2014) Evaluating heterogeneity of sex-specific capture probability and precision in camera-trap population estimates of tigers. Wildlife Society Bulletin, 38, 791796.
Sollmann, R., Malzoni, M., Gardner, B., Hofer, H., Jácomo, A.T.A., Mundim, N. & Silveira, L. (2011) Improving density estimates for elusive carnivores: accounting for sex-specific detection and movements using spatial capture–recapture models for jaguars in central Brazil. Biological Conservation, 144, 10171024.
Sollmann, R., Gardner, B. & Belant, J.L. (2012) How does spatial study design influence density estimates from spatial capture-recapture models? PLOS ONE, 7, e34575.
Sollmann, R., Linkie, M., Haidir, I.A. & Macdonald, D.W. (2014) Bringing clarity to the clouded leopard Neofelis diardi: first density estimates from Sumatra. Oryx, 48, 536539.
Sun, C.C., Fuller, A.K. & Royle, J.A. (2014) Trap configuration and spacing influences parameter estimates in spatial capture–recapture models. PLOS ONE, 9, e88025.
Sunarto, , Sanderson, J. & Wilting, A. (2008) Neofelis diardi ssp. diardi. In The IUCN Red List of Threatened Species 2008: e.T136866A4347690. http://dx.doi.org/10.2305/IUCN.UK.2008.RLTS.T136866A4347690.en [accessed 15 July 2017].
Tobler, M.W. & Powell, G.V.N. (2013) Estimating jaguar densities with camera traps: problems with current designs and recommendations for future studies. Biological Conservation, 159, 109118.
Tobler, M.W., Carrillo-Percastegui, S.E., Zúñiga Hartley, A. & Powell, G.V.N. (2013) High jaguar densities and large population sizes in the core habitat of the southwestern Amazon. Biological Conservation, 159, 375381.
Wearn, O.R., Rowcliffe, J.M., Carbone, C., Bernard, H. & Ewers, R.M. (2013) Assessing the status of wild felids in a highly-disturbed commercial forest reserve in Borneo and the implications for camera trap survey design. PLOS ONE, 8, e77598.
Wilting, A., Mohamed, A., Ambu, L.N., Lagan, P., Mannan, S., Hofer, H. & Sollmann, R. (2012) Density of the Vulnerable Sunda clouded leopard Neofelis diardi in two commercial forest reserves in Sabah, Malaysian Borneo. Oryx, 46, 423426.
Wilton, C.M., Puckett, E.E., Beringer, J., Gardner, B., Eggert, L.S. & Belant, J.L. (2014) Trap array configuration influences estimates and precision of black bear density and abundance. PLOS ONE, 9, e111257.
Zimmermann, F., Breitenmoser-Würsten, C., Molinari-Jobin, A. & Breitenmoser, U. (2013) Optimizing the size of the area surveyed for monitoring a Eurasian lynx (Lynx lynx) population in the Swiss Alps by means of photographic capture–recapture. Integrative Zoology, 8, 232243.

Keywords

Type Description Title
PDF
Supplementary materials

Mohamed et al. supplementary material
Tables S1-S3

 PDF (145 KB)
145 KB

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed