Using occupancy-based camera-trap surveys to assess the Critically Endangered primate Macaca nigra across its range in North Sulawesi, Indonesia
CASPIA N L. JOHNSON,HARR Y HIL SE R,MATTHEW L IN KI E,RIV O RAHASIA FRANCESCO ROVE R O,WULAN P USP A RINI ,IWAN HUNOWU ALFON S P ATA N D U N G,NOVI A R ANDAYAN I ,JOHN TASIRI N L UKITA A. NISTYANTA RA and ANDREW E. BOWK E T T
Abstract Primates are one of the most threatened groups of mammals. Understanding their patterns of population oc- currence and abundance, especially in response to threats, is critical for informing conservation action. The crested black macaque Macaca nigra is the only Critically En- dangered species of Sulawesi’s seven endemic macaques. Little is known about its distribution or its response to deforestation and hunting. We conducted a camera-trap survey across the entire species range using an occupancy- based analytical approach to (1) establish the first range- wide baseline of occurrence, (2) investigate how environ- mental and anthropogenic factors influence occurrence, (3) identify priority conservation subpopulations, and (4) test the efficacy of the sampling and analytical protocol for temporal monitoring of M. nigra using occupancy as the state variable. From 9,753 camera-trap days, M. nigra was detected on 473 days at 77 of the 111 camera locations. Species occupancy was 0.66 and highest inside protected areas and closed canopy forest. We identified eight distinct subpopulations, based on distribution and forest fragment size. To inform future monitoring, we used a power analysis to determine if our effort would allow us to detect inter- annual occupancy declines of 10%, and found that 90
CASPIAN L. JOHNSON* (Corresponding author,
orcid.org/0000-0001-6990-
7952) Selamatkan Yaki Foundation, Manado, Indonesia E-mail
caspianjohnson@gmail.com
HARRY HILSER† Selamatkan Yaki Foundation, Manado, Indonesia
MATTHEW LINKIE,WULAN PUSPARINI,IWAN HUNOWU,ALFONS PATANDUNG and NOVIAR ANDAYANI Wildlife Conservation Society, Bogor, Indonesia
RIVO RAHASIA‡ Natural Resource Conservation Agency, North Sulawesi, Indonesia
FRANCESCO ROVERO§ Tropical Biodiversity Section, Museo delle Scienze, Trento, Italy JOHN TASIRIN University of Sam Ratulangi, Manado, Indonesia LUKITA A. NISTYANTARA BOGANI¶ Nani Wartabone National Park ANDREW E. BOWKETT Whitley Wildlife Conservation Trust, Paignton, UK
*Also at: Bristol Zoological Society, Bristol, UK †Also at: Department of Geography, Exeter University, Exeter, UK ‡Also at: Selamatkan Yaki Foundation, Manado, Indonesia §Also at: Department of Biology, University of Florence, Florence, Italy ¶Also at: Natural Resource Conservation Agency, North Sulawesi, Indonesia
Received 8 February 2019. Revision requested 15 April 2019. Accepted 15 July 2019. First published online 29 September 2020.
camera locations surveyed for 3 months (8,100 camera days) across three consecutive seasons is the effort required to de- tect such change with 80%certainty. Our study underscores the importance of well-managed protected areas and intact forests for the long-term survival of the crested black ma- caque, and tests the effectiveness of camera traps to monitor primates at the landscape scale.
Keywords Camera trap, presence–absence, Macaca nigra, occupancy, power analysis, primates, detectability, cost– benefit, modelling
Supplementary material for this article is available at
doi.org/10.1017/S0030605319000851
Introduction
IUCN Red List), with 75% of all primate species being in a state of decline (Estrada et al., 2017). The threats to primate species are broad and wide-ranging,withmany acting in syn- ergy to hasten population declines, but hunting for trade and habitat loss from logging and agricultural expansion are the primary drivers (Cowlishaw & Dunbar, 2000; Estrada et al., 2017). To understand the effects of threats on primate popu- lations, bespoke monitoring programmes are critical. Monitoring of primate populations provides forewarn-
G
ing of declines and, by recognizing causal factors, a good monitoring programme can identify mitigating solutions. However, monitoring primates using abundance metrics can be resource intensive and time consuming at large spatial scales (Walsh & White, 1999; Cavada et al., 2017), especially if the focal species are hunted and therefore wary of humans, or live in remote and inaccessible locations (Fashing & Cords, 2000). To address this, several recent studies have recommended using occupancy as the state variable, rather than abundance, as a more cost-effective option (Sanje mangaby Cercocebus sanjei,Rovero etal., 2014;indri Indri indri,Keane et al., 2012; Alaotra reed lemur Hapalemur alaotrensis,Guillera-Arroitaetal., 2010). Occupancy modelling corrects for detectability issues by using presence/absence (detection/non-detection) data to
Oryx, 2020, 54(6), 784–793 © The Author(s), 2020. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605319000851
lobally, an estimated 60% of primate species are at risk of extinction (i.e. categorized as threatened on the
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