Animal Conservation.

Print ISSN 1367-9430

RESPONSE

Further notes on the analysis of mammal inventory data collected with camera traps
M. W. Tobler1,2, S. E. Carrillo-Percastegui3, R. Leite Pitman4, R. Mares3 & G. Powell3
1 Botanical Research Institute of Texas, Andes to Amazon Biodiversity Program, Fort Worth, TX, USA 2 Texas A&M University, Department of Wildlife and Fisheries Sciences, College Station, TX, USA 3 World Wildlife Fund, Washington, DC, USA 4 Duke University Center for Tropical Conservation , Instituto Procarnivoros, Oxford University Wildlife and Research Conservation Unit, Durham, NC, USA

Correspondence Mathias W. Tobler, Botanical Research Institute of Texas, 509 Pecan Street, Fort Worth, TX 76102-4060, USA. Email: matobler@brit.org

doi:10.1111/j.1469-1795.2008.00181.x

The use of camera traps has drastically increased over the last years (Rowcliffe & Carbone, 2008), and a large amount of data are being collected from sites all over the world. However, most studies only publish a small subset of the collected data, usually focusing on only one or two species. The example of capturerecapture studies using camera traps shows how the availability of a clear methodology and guidelines for study designs (Karanth & Nichols, 1998) can result in a large number of researchers adopting the methodology for a range of species (e.g. Noss, Pena & Rumiz, 2004; Silver et al., 2004, Jackson et al., 2006; Trolle et al., 2008). At the same time, the use of a standard methodology across studies allows for easy comparisons between sites (e.g. Karanth & Nichols, 1998; Silver et al., 2004; Kelly et al., 2008). Our article (Tobler et al., 2008) presents different methods for analyzing and presenting species inventory data collected with camera traps and addresses various design issues. We hope that this will encourage others to analyze and publish newly collected or already available data on mammal communities from different sites. Following the suggestion by OBrien (2008), we tested the performance of occupancy models for species richness estimation with our data. We followed the guidelines given in MacKenzie et al. (2006: pp. 250253) and tested four different models (1) a single season model with constant detection probability (SS); (2) a single season model with survey-specic detection probabilities (SS time); (3) a twogroup nite mixture model (FM2); (4) the RoyleNichols model (RN). Occupancy models use presence/absence data from multiple surveys to estimate detection probabilities. We combined data from six camera trap days for one survey occasion which resulted in 10 survey occasions used in the analysis of each dataset. The total number of species

possibly present was set to 28, according to a species list based on direct and indirect observations made by various researchers during or shortly before and after the camera trap surveys. We evaluated the effect of sample size by using subsamples of the data. We analyzed the data in the order they were collected without randomization, so that results differ from the ones given in table 3 in Tobler et al. (2008). All occupancy models were calculated with Presence (Hines, 2007) and Jackknife estimators were calculated with EstimateS (Colwell, 2006). Model selection based on the Akaike information criterion (AIC) selected the FM2 model as best model for both datasets, followed by the RN model (Table 1).

Table 1 Summary statistics for ve occupancy models used to estimate species diversity from camera trap data Model 2005 FM2 RN SS SS time 2006 FM2 RN SS SS time AIC 278.4 286.3 326.3 337.6 280.8 290.5 348.3 364.2 DAIC 0.0 7.9 47.9 59.2 0.0 9.7 67.5 83.4 w 0.98 0.02 0.00 0.00 0.99 0.01 0.00 0.00 N Par. 4 2 2 11 4 2 2 11 2l 270.4 282.3 322.3 315.6 272.8 286.5 344.3 342.2

FM2, two-group nite mixture model; RN, RoyleNichols model; SS, single season model with constant p; SS time, single season model with survey specic p. DAIC is the difference in AIC values between each model and the best model and w is the AIC model weight, N Par is the number of parameters and 2l is twice the negative log-likelihood.

c 2008 The Authors. Journal compilation c 2008 The Zoological Society of London Animal Conservation 11 (2008) 187189

187

Analysis of mammal inventory data from camera traps

M. W. Tobler et al.

Table 2 Observed and estimated species richness under different sampling intensity for two camera trap surveys in the Peruvian Amazon 2005 Days Camera days Sobs SS FM2 RN Jack 1 Jack 2 12 288 16 19 19 21 24 31 24 576 20 21 27 22 29 36 36 864 21 21 25 23 28 32 48 1152 21 21 a 23 26 29 60 1440 21 21 26 23 26 29 2006 12 468 17 18 19 19 22 24 24 936 20 20 23 21 27 31 36 1404 23 23 24 26 29 35 48 1872 24 24 27 26 30 36 60 2340 24 24 27 25 27 27

Sobs, observed number of species; SS, single season model with constant p; FM2, two-group nite mixture model; RN, RoyleNichols model; Jack 1, rst order Jackknife estimator; Jack 2, second order Jackknife estimator. The number of species believed to be present in the study area is 28. aThe maximum likelihood estimator did not converge for this model.

Selection of these particular models indicates that the data contains a high level of heterogeneity, something we would expect with camera trap data from a wide range of species. The FM2 model gave the best estimates of the three occupancy models while the SS model hardly differed from the observed number of species (Sobs) (Table 2). The Jackknife estimators performed better than Sobs as we have shown before (Tobler et al., 2008) but showed more variance than the FM2 model. One drawback of the occupancy models tested here is that the total number of species that can possibly occur at a site needs to be known from a regional species list. The model then estimates the fraction of species that is actually present at the site. However, regional species lists are not always available or complete. Future studies need to evaluate how sensitive these models are with regard to the value chosen for the total number of species. The usefulness of capture frequencies as an index for abundance was not the topic of our article; however, we briey addressed the issue in the discussion of our results. Kelly et al. (2008) correctly pointed out that capture frequencies were highly correlated between surveys and suggests that the usefulness of capture frequencies as an index should be explored. However, this analysis includes frequencies from all species spanning two orders of magnitude (0.466) and does not give any information on the relationship between abundance and capture frequencies. It cannot be determined whether an increase of the capture frequency from 5.6 to 13.2 for the red brocket deer Mazama americana really reects a population increase, nor if the decline of the capture frequency from 16.0 to 8.1 for the collared peccary Pecary tajacu reects a population decline. We agree that there exists a relationship between abundance and capture frequencies, however, as pointed out by Tobler et al. (2008) and Rowcliffe & Carbone (2008), there are several other factors that inuence capture probability and that can confound the relationship. In order to compare data between species, surveys or study sites the capture probability needs to be estimated from the data. Rowcliffe & Carbone (2008) refer to a new method they recently developed to address this problem. Another promising approach is to use occupancy as a surrogate for abundance
188

(MacKenzie & Nichols, 2004), and to use occupancy models to estimate capture probabilities (MacKenzie et al., 2006). Occupancy models are very exible and allow the inclusion of covariates to test for difference in occupancy rates between sites or habitats and multi-season models can be used to look at extinction and colonization rate. However, despite their great potential, so far they have only rarely been applied to camera trap data (e.g. MacKenzie et al., 2005; Linkie et al., 2007). We hope that our results will encourage others to investigate possible new ways of analyzing camera trap data. As pointed out by Rowcliffe & Carbone (2008), many interesting questions could be addressed based on existing data if all these data were organized and presented in a more standardized way. We are convinced that advances in camera technology together with better designs and new methods and software for data analysis will allow camera trap studies to address an even broader range of questions, thus making them one of the most versatile tools available to biologists.

References
Colwell, R.K. (2006). Estimates: statistical estimation of species richness and shared species from samples, Version 8.0. http://purl.oclc.org/estimates Hines, J.E. (2007). Presene 2.1 software to estimate patch occupancy and related parameters: USGS-PWRC, http:// www.mbr-pwrc.usgs.gov/software/presence.html Jackson, R.M., Roe, J.D., Wangchuk, R. & Hunter, D.O. (2006). Estimating snow leopard population abundance using photography and capturerecapture techniques. Wildl. Soc. Bull. 34, 772781. Karanth, K.U. & Nichols, J.D. (1998). Estimation of tiger densities in India using photographic captures and recaptures. Ecology 79, 28522862. Kelly, M.J., Noss, A.J., di Bitetti, M.S., Maffei, L., Arispe, R.L., Paviolo, A., De Angelo, C.D. & Di Blanco, Y.E. (2008). Estimating puma densities from camera trapping across three study sites: Bolivia, Argentina, and Belize. J. Mammal. 89, 408418.

c 2008 The Authors. Journal compilation c 2008 The Zoological Society of London Animal Conservation 11 (2008) 187189

M. W. Tobler et al.

Analysis of mammal inventory data from camera traps

Linkie, M., Dinata, Y., Nugroho, A. & Haidir, I.A. (2007). Estimating occupancy of a data decient mammalian species living in tropical rainforests: Sun bears in the Kerinci Seblat region, Sumatra. Biol. Conserv. 137, 2027. Mackenzie, D.I. & Nichols, J.D. (2004). Occupancy as a surrogate for abundance estimation. Anim. Biodivers. Conserv. 27, 461467. Mackenzie, D.I., Nichols, J.D., Sutton, N., Kawanishi, K. & Bailey, L.L. (2005). Improving inferences in population studies of rare species that are detected imperfectly. Ecology 86, 11011113. Mackenzie, D.I., Nichols, J.D., Royle, J.A., Pollock, K.H., Bailey, L.L. & Hines, J.E. (2006). Occupancy estimation and modeling: inferring patterns and dynamics of species occurrence. Amsterdam: Elsevier. Noss, A.J., Pena, R. & Rumiz, D.I. (2004). Camera trapping Priodontes maximus in the dry forests of Santa Cruz, Bolivia. Endangered Species UPDATE 21, 4352.

OBrien, T.G. (2008). On the use of automated cameras to estimate species richness for large and medium-sized rainforest mammals. Anim. Conserv. 11, 179181. Rowcliffe, J.M. & Carbone, C. (2008). Surveys using camera traps: are we looking to a brighter future? Anim. Conserv. 11, 185186. Silver, S.C., Ostro, L.E.T., Marsh, L.K., Maffei, L., Kelly, A.M.J., Wallace, R.B., Gomez, H. & Ayala, G. (2004). The use of camera traps for estimating jaguar Panthera onca abundance and density using capture/recapture analysis. Oryx 38, 148154. Tobler, M.W., Carrillo-Percastegui, S.E., Leite Pitman, R., Mares, R. & Powell, G. (2008). An evaluation of camera traps for inventorying large and medium sized terrestrial rainforest mammals. Anim. Conserv. 11, 169178. Trolle, M., Noss, A.J., Cordeiro, J.L.P. & Oliveira, L.F.B. (2008). Brazilian tapir density in the pantanal: a comparison of systematic camera-trapping and line-transect surveys. Biotropica 40, 211217.

c 2008 The Authors. Journal compilation c 2008 The Zoological Society of London Animal Conservation 11 (2008) 187189

189