The Habituation Process in Two Groups of Wild Moor Macaques (Macaca maura)

Abstract

When studying animal behavior in the wild, some behaviors may require observation from a relatively short distance. In these cases, habituation is commonly used to ensure that animals do not perceive researchers as a direct threat and do not alter their behavior in their presence. However, habituation can have significant effects on the welfare and conservation of the animals. Studying how nonhuman primates react to the process of habituation can help to identify the factors that affect habituation and implement habituation protocols that allow other researchers to speed up the process while maintaining high standards of health and safety for both animals and researchers. In this study, we systematically described the habituation of two groups of wild moor macaques (Macaca maura), an Endangered endemic species of Sulawesi Island (Indonesia), to assess the factors that facilitate habituation and reduce impact on animal behavior during this process. During 7 months, we conducted behavioral observations for more than 7,872 encounters and an average of 120 days to monitor how macaque behavior toward researchers changed through time in the two groups under different conditions. We found that both study groups (N = 56, N = 41) became more tolerant to the presence of researchers during the course of the habituation, with occurrence of neutral group responses increasing, and minimum distance to researchers and occurrence of fearful group responses decreasing through time. These changes in behavior were predominant when macaques were in trees, with better visibility conditions, when researchers maintained a longer minimum distance to macaques and, unexpectedly, by the presence of more than one researcher. By identifying these factors, we contribute to designing habituation protocols that decrease the likelihood of fearful responses and might reduce the stress experienced during this process.

Social dynamics of vervet monkeys are dependent upon group identity

“…This result could be due to the gradual habituation of vervets to human presence, where habituation is defined as “the process by which repeated exposure to humans results in a gradual reduction in animals’ fearful response, until animals no longer perceive humans as a direct threat”. 97 At the start of our study in 2012, the three groups were less habituated to observers so human presence might have stressed monkeys, impacted their behavior and generated more conflicts. Data collection was also more difficult compared to nine years later where monkeys were highly habituated to human presence.…”

A review of Gabonese gorillas and their pathogens: Diversity, transfer and One Health approach to avoid future outbreaks?

“…It is, therefore, to be feared that with Gabonese government policies aimed at promoting ecotourism and then research and mining activities that will accentuate contacts between wildlife, particularly gorillas, and humans, the exchange of pathogens will be more frequent. This provides ample justification for implementing a One Health approach, mainly since gorilla habituation projects are being conducted in some of Gabon's thirteen national parks (Hernańdez Tienda et al, 2022), like in Loango National Park (Oelze et al, 2014;Hernańdez Tienda et al, 2022) or Moukalaba Doudou National Park (Ando et al, 2008). The One Health approach must prevent and control any emergence, re-emergence, or spread/dissemination of zoonotic pathogens harbored by Gabonese gorillas.…”

Moor Macaques (Macaca maura) Remember Earlier Habituation Despite Changes in Group Composition

“…The time needed to successfully habituate study animals depends on several factors, including their socioecological characteristics, personality, and previous experience with humans (Allan et al, 2020;Williamson & Feistner, 2011). For example, animals that have previously experienced neutral exposure to humans may habituate more quickly than animals that have rarely encountered or have been threatened by humans (Sak et al, 2013;Hernandez-Tienda et al, 2022).Very few empirical data exist concerning whether, or for how long, animals remain habituated when they are not continuously exposed to researchers. If the memory of habituation is long-term, animals should remain habituated after a period with no exposure to researchers.…”

“…The time needed to successfully habituate study animals depends on several factors, including their socioecological characteristics, personality, and previous experience with humans (Allan et al, 2020;Williamson & Feistner, 2011). For example, animals that have previously experienced neutral exposure to humans may habituate more quickly than animals that have rarely encountered or have been threatened by humans (Sak et al, 2013;Hernandez-Tienda et al, 2022).…”

“…The outbreak of COVID-19 in 2020 provided us with the rare opportunity to test these predictions on a wild group of moor macaques (Macaca maura), which are endemic to Sulawesi, Indonesia. Our study group was located at Bara Beach (5°36'S, 120°26'E), South Sulawesi, in a seaside limestone secondary forest area of around 415,000 ha with access to cultivated fields and beaches (Hernandez-Tienda et al, 2022). The group was first habituated (phase 1) from October 2019 to March 2020 (Hernandez-Tienda et al, 2022), when it consisted of 41 individuals (6 adult males, 13 adult females and 22 immatures).…”