Register      Login
Wildlife Research Wildlife Research Society
Ecology, management and conservation in natural and modified habitats
RESEARCH ARTICLE

Elusive species and where to find them: assessment of survey protocols for primates habitat selection

Eva Gazagne https://orcid.org/0000-0001-8077-4193 A * , Moïra Wilputte C , Dusit Ngoprasert B , Martine Vercauteren C , Régine Vercauteren Drubbel C and Tommaso Savini B
+ Author Affiliations
- Author Affiliations

A Unit of Research SPHERES, University of Liège, Quai van Beneden, 22, Liège 4020, Belgium.

B Conservation Ecology Program, King Mongkut’s University of Technology Thonburi, 49 Soi Tienthalay, 25 Bangkhuntien-Chaithalay Road, Thakham, Bangkhuntien 10150, Thailand.

C Unit of Anthropology and Human Genetics, Free University of Brussels, Avenue F.D. Roosevelt, 50, Brussels 1050, Belgium.

* Correspondence to: evagazagne@live.fr

Handling Editor: Cristián F. Estades

Wildlife Research 51, WR21116 https://doi.org/10.1071/WR21116
Submitted: 4 August 2021  Accepted: 9 March 2023  Published: 4 April 2023

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Context

With the ongoing biodiversity crisis and the continued loss of species, it becomes crucial to find practical solutions to monitor threatened animal populations for wildlife conservation and management. However, in practice, monitoring is especially challenging for elusive, rare, and wide-ranging species, where estimating abundance is often expensive and time-consuming. Alternatively, estimating occupancy (i.e. detection/non-detection data) may be less resource-intensive, while still providing useful information for monitoring population trends.

Aims

We aimed to describe a new field method, the random walk grid survey, to conduct a habitat selection study on elusive diurnal forest-dwelling primates. We explored how to improve occupancy estimates when detection probability is low and determined the minimal effort needed for reasonable estimates on the species habitat selection by using site-occupancy models.

Methods

We collected data to assess the northern pigtailed macaques’ (Macaca leonina) occupancy and detection probability using a random walk survey of degraded forest fragments in Sakaerat Biosphere Reserve in Northeast Thailand. We ran simulations to identify what is required for minimum survey efforts to obtain reasonable estimates of occupancy and detection probability on small or relatively large spatial scales, covering a small primate community in Southeast Asia.

Key results

Simulations showed that the probability of detecting macaques increased dramatically with an increased survey effort. However, compared with similar line-transect survey methods, the random walk grid survey was less time-consuming. Additionally, the occupancy and habitat selection estimates were similar to our knowledge of macaque distribution within the study area.

Conclusions

Our findings suggest that the new random walk grid survey method is effective to assess the elusive northern pigtailed macaques’ occupancy, and to provide reliable data on habitat selection where there is low macaque abundance and detection probability in a degraded forest fragment.

Implications

Our survey protocol could be used as a starting point to target high location occupancy to start habituation processes, but also for further intensive studies on primate behaviour and habitat use of primate communities. Finally, combining the random walk grid survey with automated recording devices (e.g. camera traps or passive acoustic surveys) could help improve occupancy and detection probability estimates for long-term monitoring programs and over large spatial scales.

Keywords: forest-dwelling primates, habitat selection, imperfect detection, Macaca leonina, random walk grid survey, simulations, site-occupancy model, survey effort.

References

Akaike H (1973) Information theory and an extension of the maximum likelihood principle. In ‘International symposium on information theory’. (Eds BN Petrov, F Czáki) pp. 267–281. (Akademiai Kiado: Budapest, Hungary)

Albert A (2012) Feeding and ranging behavior of northern pigtailed macaques (Macaca leonina): impact on their seed dispersal effectiveness and ecological contribution in a tropical rainforest at Khao Yai National Park, Thailand. PhD. Thesis, University of Liège, Belgium. Available at https://hdl.handle.net/2268/108250

Baker LR, Arnold TW, Olubode OS, Garshelis DL (2011) Considerations for using occupancy surveys to monitor forest primates: a case study with sclater’s monkey (Cercopithecus sclateri). Population Ecology 53(4), 549-561.
| Crossref | Google Scholar |

Bertolani P, Boesch C (2008) Habituation of wild chimpanzees (Pan troglodytes) of the South Group at Taï Forest, Côte d’Ivoire: empirical measure of progress. Folia Primatologica 79(3), 162-171.
| Crossref | Google Scholar |

Bled F, Belant JL, Van Daele LJ, Svoboda N, Gustine D, Hilderbrand G, Barnes VG, Jr. (2017) Using multiple data types and integrated population models to improve our knowledge of apex predator population dynamics. Ecology and Evolution 7(22), 9531-9543.
| Crossref | Google Scholar |

Borries C, Larney E, Kreetiyutanont K, Koenig A (2002) The diurnal primate community in a dry evergreen forest in Phu Khieo Wildlife Sanctuary, Northeast Thailand. Natural History Bulletin of the Siam Society 50(1), 75-88.
| Google Scholar |

Bowler MT, Tobler MW, Endress BA, Gilmore MP, Anderson MJ (2017) Estimating mammalian species richness and occupancy in tropical forest canopies with arboreal camera traps. Remote Sensing in Ecology and Conservation 3(3), 146-157.
| Crossref | Google Scholar |

Brassine E, Parker D (2015) Trapping elusive cats: using intensive camera trapping to estimate the density of a rare African felid. PLoS ONE 10(12), e0142508.
| Crossref | Google Scholar |

Brodie JF, Helmy O, Pangau-Adam M, Ugiek G, Froese G, Granados A, Mohd-Azlan J, Bernard H, Giordano AJ, Agil M, Haris Mustari A (2018) Crossing the (Wallace) line: local abundance and distribution of mammals across biogeographic barriers. Biotropica 50, 116-124.
| Crossref | Google Scholar |

Buckland ST, Plumptre AJ, Thomas L, Rexstad EA (2010) Design and analysis of line transect surveys for primates. International Journal of Primatology 31(5), 833-847.
| Crossref | Google Scholar |

Burnham KP, Anderson DR (Eds) (2002) ‘Model Selection and Multimodel Inference: a Practical Information–Theoretic Approach, Vol. 2.’ (Springer: New York)

Campbell N, Nekaris KAI, Pereira TS, Allgas N, Shanee S (2019) Occupancy modeling for the conservation assessment of the Peruvian night monkey (Aotus miconax). Primate Conservation 33, 13-20.
| Google Scholar |

Coelho IP, Collins SJ, Santos Junior EM, Valença-Montenegro MM, Jerusalinsky L, Alonso AC (2020) Playback point counts and N-mixture models suggest higher than expected abundance of the critically endangered blond titi monkey in northeastern Brazil. American Journal of Primatology 82(5), e23126.
| Crossref | Google Scholar |

Crunchant A-S, Borchers D, Kühl H, Piel A (2020) Listening and watching: do camera traps or acoustic sensors more efficiently detect wild chimpanzees in an open habitat? Methods in Ecology and Evolution 11(4), 542-552.
| Crossref | Google Scholar |

Doran-Sheehy DM, Derby AM, Greer D, Mongo P (2007) Habituation of western gorillas: the process and factors that influence it. American Journal of Primatology 69(12), 1354-1369.
| Crossref | Google Scholar |

Estrada A, Garber PA, Rylands AB, Roos C, Fernandez-Duque E, Di Fiore A, et al. (2017) Impending extinction crisis of the world’s primates: why primates matter. Science Advances 3(1), e1600946.
| Crossref | Google Scholar |

Farris ZJ, Chan S, Rafaliarison R, Valenta K (2019) Occupancy modeling reveals interspecific variation in habitat use and negative effects of dogs on lemur populations. International Journal of Primatology 40(6), 706-720.
| Crossref | Google Scholar |

Fiske I, Chandler R (2011) Unmarked: an R package for fitting hierarchical models of wildlife occurrence and abundance. Journal of Statistical Software 43(10), 1-23.
| Crossref | Google Scholar |

Gálvez N, Guillera-Arroita G, Morgan BJT, Davies ZG (2016) Cost-efficient effort allocation for camera-trap occupancy surveys of mammals. Biological Conservation 204, 350-359.
| Crossref | Google Scholar |

Gazagne E, Hambuckers A, Savini T, Poncin P, Huynen M-C, Brotcorne F (2020a) Toward a better understanding of habituation process to human observer: a statistical approach in Macaca leonina (Primates: Cercopithecidea). Raffles Bulletin of Zoology 68, 735-749.
| Crossref | Google Scholar |

Gazagne E, José-Domínguez JM, Huynen M-C, Hambuckers A, Poncin P, Savini T, Brotcorne F (2020b) Northern pigtailed macaques rely on old growth plantations to offset low fruit availability in a degraded forest fragment. American Journal of Primatology 82(5), e23117.
| Crossref | Google Scholar |

Gelman A, Hill J (2007) ‘Data Analysis Using Regression and Multilevel/Hierarchical Models.’ (Cambridge University Press: NY, USA)

Gerber BD, Williams PJ, Bailey LL (2014) Primates and cameras. International Journal of Primatology 35(5), 841-858.
| Crossref | Google Scholar |

Gillespie GR, Fukuda Y, McDonald P (2020) Using non-systematically collected data to evaluate the conservation status of elusive species: a case study on Australia’s Oenpelli python. Wildlife Research 47(2), 146-157.
| Crossref | Google Scholar |

Gnanaolivu SD, Kumara HN, Singh M, Sudarsanam D (2020) Ecological determinants of Malabar Slender Loris (Loris lydekkerianus malabaricus, Cabrera 1908) Occupancy and abundance in Aralam Wildlife Sanctuary, Western Ghats, India. International Journal of Primatology 41(3), 511-524.
| Crossref | Google Scholar |

Guillera-Arroita G, Lahoz-Monfort JJ (2012) Designing studies to detect differences in species occupancy: power analysis under imperfect detection. Methods in Ecology and Evolution 3(5), 860-869.
| Crossref | Google Scholar |

Guillera-Arroita G, Ridout MS, Morgan BJT (2010a) Design of occupancy studies with imperfect detection. Methods in Ecology and Evolution 1(2), 131-139.
| Crossref | Google Scholar |

Guillera-Arroita G, Lahoz-Monfort JJ, Milner-Gulland EJ, Young RP, Nicholson E (2010b) Using occupancy as a state variable for monitoring the Critically Endangered Alaotran gentle lemur Hapalemur alaotrensis. Endangered Species Research 11(2), 157-166.
| Crossref | Google Scholar |

Hallam CD, Johnson A, O’Kelly H, Seateun S, Thamsatith T, O’Brien TG, Strindberg S (2016) Using occupancy-based surveys and multi-model inference to estimate abundance and distribution of crested gibbons (Nomascus spp.) in central Laos. American Journal of Primatology 78(4), 462-472.
| Crossref | Google Scholar |

Hanson KT, Riley EP (2018) Beyond neutrality: the human–primate interface during the habituation process. International Journal of Primatology 39(5), 852-877.
| Crossref | Google Scholar |

Ismaila N, Maloueki U (2021) Gorilla abundance estimations within North-East Moukalaba-Doudou National Park, Gabon. Folia Primatologica 92(2), 103-111.
| Crossref | Google Scholar |

Johnson CL, Hilser H, Linkie M, Rahasia R, Rovero F, Pusparini W, et al. (2020) Using occupancy-based camera-trap surveys to assess the Critically Endangered primate Macaca nigra across its range in North Sulawesi, Indonesia. Oryx 54(6), 784-793.
| Crossref | Google Scholar |

José-Domínguez JM, Savini T, Asensio N (2015a) Ranging and site fidelity in northern pigtailed macaques (Macaca leonina) over different temporal scales. American Journal of Primatology 77(8), 841-853.
| Crossref | Google Scholar |

José-Domínguez JM, Asensio N, García CJG, Huynen M-C, Savini T (2015b) Exploring the multiple functions of sleeping sites in northern pigtailed macaques (Macaca leonina). International Journal of Primatology 36(5), 948-966.
| Crossref | Google Scholar |

Joseph LN, Field SA, Wilcox C, Possingham HP (2006) Presence–absence versus abundance data for monitoring threatened species. Conservation Biology 20(6), 1679-1687.
| Crossref | Google Scholar |

Kalan AK, Mundry R, Wagner OJJ, Heinicke S, Boesch C, Kühl HS (2015) Towards the automated detection and occupancy estimation of primates using passive acoustic monitoring. Ecological Indicators 54, 217-226.
| Crossref | Google Scholar |

Karanth KK, Nichols JD, Hines JE (2010) Occurrence and distribution of Indian primates. Biological Conservation 143(12), 2891-2899.
| Crossref | Google Scholar |

Keane A, Jones JPG, Milner-Gulland EJ (2011) Encounter data in resource management and ecology: pitfalls and possibilities. Journal of Applied Ecology 48(5), 1164-1173.
| Crossref | Google Scholar |

Keane A, Hobinjatovo T, Razafimanahaka HJ, Jenkins RKB, Jones JPG (2012) The potential of occupancy modelling as a tool for monitoring wild primate populations. Animal Conservation 15(5), 457-465.
| Crossref | Google Scholar |

Khamcha D, Powell LA, Gale GA (2018) Effects of roadside edge on nest predators and nest survival of Asian tropical forest birds. Global Ecology and Conservation 16, e00450.
| Crossref | Google Scholar |

Kühl H, Maisels F, Ancrenaz M, Williamson EA (2008) ‘Best Practice Guidelines for Surveys and Monitoring of Great Ape Populations.’ (IUCN/SSC Primate Specialist Group: Gland, Switzerland)

MacKenzie DI, Reardon JT (2013) Occupancy methods for conservation management. In ‘Biodiversity Monitoring and Conservation: Bridging the Gap Between Global Commitment and Local Action’. (Eds B Collen, N Pettorelli, JEM Baillie, SM Durant) pp. 248–264. (John Wiley and Sons, Ltd: Hoboken, NJ, United States)

MacKenzie DI, Royle JA (2005) Designing occupancy studies: general advice and allocating survey effort. Journal of Applied Ecology 42, 1105-1114.
| Crossref | Google Scholar |

MacKenzie DI, Nichols JD, Lachman GB, Droege S, Andrew Royle J, Langtimm CA (2002) Estimating site occupancy rates when detection probabilities are less than one. Ecology 83(8), 2248-2255.
| Crossref | Google Scholar |

MacKenzie DI, Nichols JD, Royle JA, Pollock KH, Bailey LL, Hines JE (2017) ‘Occupancy Estimation and Modeling: Inferring Patterns and Dynamics of Species Occurrence.’ 2nd edn. (Academic Press – Elsevier: Cambridge, USA) doi:10.1016/c2012-0-01164-7

Martin J, Chamaillé-Jammes S, Nichols JD, Fritz H, Hines JE, Fonnesbeck CJ, MacKenzie DI, Bailey LL (2010) Simultaneous modeling of habitat suitability, occupancy, and relative abundance: African elephants in Zimbabwe. Ecological Applications 20(4), 1173-1182.
| Crossref | Google Scholar |

McKelvey KS, Aubry KB, Schwartz MK (2008) Using anecdotal occurrence data for rare or elusive species: the illusion of reality and a call for evidentiary standards. BioScience 58(6), 549-555.
| Crossref | Google Scholar |

Morant J, González-Oreja JA, Martínez JE, López-López P, Zuberogoitia I (2020) Applying economic and ecological criteria to design cost-effective monitoring for elusive species. Ecological Indicators 115, 106366.
| Crossref | Google Scholar |

Morris DW (2003) How can we apply theories of habitat selection to wildlife conservation and management? Wildlife Research 30(4), 303-319.
| Crossref | Google Scholar |

Murphy A, Kelly MJ, Karpanty SM, Andrianjakarivelo V, Farris ZJ (2019) Using camera traps to investigate spatial co-occurrence between exotic predators and native prey species: a case study from northeastern Madagascar. Journal of Zoology 307(4), 264-273.
| Crossref | Google Scholar |

Nafus MG, Mazzotti FJ, Reed RN (2020) Estimating detection probability for Burmese pythons with few detections and zero recaptures. Journal of Herpetology 54(1), 24-30.
| Crossref | Google Scholar |

Neilson E, Nijman V, Nekaris KAI (2013) Conservation assessments of arboreal mammals in difficult terrain: occupancy modeling of pileated gibbons (Hylobates pileatus). International Journal of Primatology 34(4), 823-835.
| Crossref | Google Scholar |

Nichols JD, Bailey LL, O’Connell AF, Jr., Talancy NW, Campbell Grant EH, Gilbert AT, et al. (2008) Multi-scale occupancy estimation and modelling using multiple detection methods. Journal of Applied Ecology 45(5), 1321-1329.
| Crossref | Google Scholar |

Nuttall M, Nut M, Ung V, O’Kelly H (2017) Abundance estimates for the Endangered green peafowl Pavo muticus in Cambodia: identification of a globally important site for conservation. Bird Conservation International 27(1), 127-139.
| Crossref | Google Scholar |

Oliver K, Ngoprasert D, Savini T (2020) Assessment of survey protocol for estimates of abundance for elusive nocturnal primates. Wildlife Research 47(5), 372-380.
| Crossref | Google Scholar |

Petersen WJ, Savini T, Gray TNE, Baker-Whatton M, Bisi F, Chutipong W, et al. (2021) Identifying conservation priorities for an understudied species in decline: Golden cats (Catopuma temminckii) in mainland Tropical Asia. Global Ecology and Conservation 30, e01762.
| Crossref | Google Scholar |

Plumptre AJ, Sterling EJ, Buckland ST (2013) Primate census and survey techniques. In ‘Primate Ecology and Conservation: a Handbook of Techniques’. (Eds EJ Sterlig, N Bynum, ME Blair) pp. 10–26. (Oxford University Press: Oxford, UK)

Plumptre AJ, Nixon S, Kujirakwinja DK, Vieilledent G, Critchlow R, Williamson EA, et al. (2016) Catastrophic decline of world’s largest primate: 80% loss of Grauer’s Gorilla (Gorilla beringei graueri) population justifies critically endangered status. PLoS ONE 11(10), e0162697.
| Crossref | Google Scholar |

QGIS Development Team (2016) QGIS geographic information system. (Open Source Geospatial Foundation Project). Available at http://qgis.osgeo.org

R Development Core Team (2021) R: a language and environment for statistical computing. Available at http://www.R-project.org [verified April 2021]

Rota CT, Ferreira MAR, Kays RW, Forrester TD, Kalies EL, McShea WJ, et al. (2016) A multispecies occupancy model for two or more interacting species. Methods in Ecology and Evolution 7(10), 1164-1173.
| Crossref | Google Scholar |

Rovero F, Martin E, Rosa M, Ahumada JA, Spitale D (2014) Estimating species richness and modelling habitat preferences of tropical forest mammals from camera trap data. PLoS ONE 9(7), e103300.
| Crossref | Google Scholar |

Royle JA (2004) N-mixture models for estimating population size from spatially replicated counts. Biometrics 60, 108-115.
| Crossref | Google Scholar |

Sales LP, Hayward MW, Passamani M (2016) Local vs landscape drivers of primate occupancy in a Brazilian fragmented region. Mammal Research 61(1), 73-82.
| Crossref | Google Scholar |

Sewell D, Guillera-Arroita G, Griffiths RA, Beebee TJC (2012) When is a species declining? Optimizing survey effort to detect population changes in reptiles. PLoS ONE 7(8), e43387.
| Crossref | Google Scholar |

Specht HM, Reich HT, Iannarilli F, Edwards MR, Stapleton SP, Weegman MD, et al. (2017) Occupancy surveys with conditional replicates: an alternative sampling design for rare species. Methods in Ecology and Evolution 8(12), 1725-1734.
| Crossref | Google Scholar |

Steenweg R, Hebblewhite M, Whittington J, Lukacs P, McKelvey K (2018) Sampling scales define occupancy and underlying occupancy–abundance relationships in animals. Ecology 99(1), 172-183.
| Crossref | Google Scholar |

Sushma HS, Ramesh KP, Kumara HN (2022) Determinants of habitat occupancy and spatial segregation of primates in the central Western Ghats, India. Primates 63(2), 137-147.
| Crossref | Google Scholar |

Suwanrat S, Ngoprasert D, Sutherland C, Suwanwaree P, Savini T (2015) Estimating density of secretive terrestrial birds (Siamese Fireback) in pristine and degraded forest using camera traps and distance sampling. Global Ecology and Conservation 3, 596-606.
| Crossref | Google Scholar |

Syxaiyakhamthor K, Ngoprasert D, Asensio N, Savini T (2020) Identifying priority areas for the conservation of the Critically Endangered northern white-cheeked gibbon Nomascus leucogenys in northern Lao. Oryx 54(6), 767-775.
| Crossref | Google Scholar |

Tagg N, Willie J (2013) The influence of transect use by local people and reuse of transects for repeated surveys on nesting in Western Lowland Gorillas (Gorilla gorilla gorilla) and Central Chimpanzees (Pan troglodytes troglodytes) in Southeast Cameroon. International Journal of Primatology 34(3), 554-570.
| Crossref | Google Scholar |

Thai Institute of Scientific and Technological Research (2017) Meteorological observations. (Sakaerat Environmental Research Station, Sakaerat Biosphere Reserves). Available at http://www.tistr.or.th/sakaerat [Accessed 13 February 2019]

Tyre AJ, Tenhumberg B, Field SA, Niejalke D, Parris K, Possingham HP (2003) Improving precision and reducing bias in biological surveys: estimating false-negative error rates. Ecological Applications 13(6), 1790-1801.
| Crossref | Google Scholar |

Vu TT, Tran LM (2019) An application of autonomous recorders for gibbon monitoring. International Journal of Primatology 40(2), 169-186.
| Crossref | Google Scholar |

Ward RJ, Griffiths RA, Wilkinson JW, Cornish N (2017) Optimising monitoring efforts for secretive snakes: a comparison of occupancy and N-mixture models for assessment of population status. Scientific Reports 7(1), 18074.
| Crossref | Google Scholar |

Warton DI, Stoklosa J, Guillera-Arroita G, MacKenzie DI, Welsh AH (2017) Graphical diagnostics for occupancy models with imperfect detection. Methods in Ecology and Evolution 8, 408-419.
| Crossref | Google Scholar |

Willcox D, Nash HC, Trageser S, Kim HJ, Hywood L, Connelly E, et al. (2019) Evaluating methods for detecting and monitoring pangolin (Pholidata: Manidae) populations. Global Ecology and Conservation 17, e00539.
| Crossref | Google Scholar |

Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods in Ecology and Evolution 1, 3-14.
| Crossref | Google Scholar |