The Implications of Primate Behavioral Flexibility for Sustainable Human–Primate Coexistence in Anthropogenic Habitats
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People are an inescapable aspect of most environments inhabited by nonhuman primates today. Consequently, interest has grown in how primates adjust their behavior to live in anthropogenic habitats. However, our understanding of primate behavioral flexibility and the degree to which it will enable primates to survive alongside people in the long term remains limited. This Special Issue brings together a collection of papers that extend our knowledge of this subject. In this introduction, we first review the literature to identify past and present trends in research and then introduce the contributions to this Special Issue. Our literature review confirms that publications on primate behavior in anthropogenic habitats, including interactions with people, increased markedly since the 2000s. Publications concern a diversity of primates but include only 17% of currently recognized species, with certain primates overrepresented in studies, e.g., chimpanzees and macaques. Primates exhibit behavioral flexibility in anthropogenic habitats in various ways, most commonly documented as dietary adjustments, i.e., incorporation of human foods including agricultural crops and provisioned items, and as differences in activity, ranging, grouping patterns, and social organization, associated with changing anthropogenic factors. Publications are more likely to include information on negative rather than positive or neutral interactions between humans and primates. The contributions to this Special Issue include both empirical research and reviews that examine various aspects of the human–primate interface. Collectively, they show that primate behavior in shared landscapes does not always conflict with human interests, and demonstrate the value of examining behavior from a cost–benefit perspective without making prior assumptions concerning the nature of interactions. Careful interdisciplinary research has the potential to greatly improve our understanding of the complexities of human–primate interactions, and is crucial for identifying appropriate mechanisms to enable sustainable human–primate coexistence in the 21st century and beyond.
KeywordsAnthropocene Behavioral adaptability Behavioral plasticity Ethnoprimatology Human-dominated landscapes Human–wildlife interactions
Flexible behavior—sometimes referred to as adaptability or plasticity, although these terms are not strictly synonyms (Strier 2017)—evolves in response to heterogeneous environments (Jones 2005). An animal’s ability to adjust its behavior under changing conditions can determine its survival in a fast-changing world dominated by humans (Wong and Candolin 2015). Until quite recently, how nonhuman primates (hereafter referred to as primates) respond behaviorally to human-induced environmental changes and increased contact with people was not a primary focus of research (cf. Horrocks and Hunte 1986; Kavanagh 1980; Maples et al. 1976 for early examples of such work). However, rapid human population growth and associated land-use changes such as agriculture and urbanization are transforming primate habitats (Estrada et al. 2012; McKinney 2015). Consequently, much field primatology today is conducted in anthropogenic habitats, a broad term that is equivalent to human-dominated or human-impacted habitats, among similar terms (see McKinney 2015 for a detailed analysis of anthropogenic influences on primate habitats). With the acceptance that modified environments offer habitat for many primates, theoretical and applied interest in how primates behave in anthropogenic habitats has increased (Hockings et al. 2015; Humle and Hill 2016; Nowak and Lee 2013; Strier 2017).
Consistent with the wider literature on human–wildlife interactions (Angelici 2016; Seoraj-Pillai and Pillay 2017; Woodroffe et al. 2005), research on primates in anthropogenic habitats has tended to concentrate on negative aspects of human–primate interactions, such as primates “raiding” agricultural crops and other “conflicts” that challenge the sustainability of primate coexistence with people (Hill 2005). This reminds us that not all behavioral adjustments to anthropogenic habitats are beneficial (Sih et al. 2011; Tuomainen and Candolin 2011; Wong and Candolin 2015), with some behaviors compromising the survival of primate populations, for example, by inciting persecution by people. Understanding primates’ behavioral flexibility in response to human influence on their habitat, and how local people perceive and respond to changing primate behavior, can inform conservation management to aid the long-term survival of primates in a fast-changing world (Hockings et al. 2015; Nowak and Lee 2013).
To explore these issues in more depth, we organized a symposium entitled “Behavioral flexibility by primates in anthropogenic habitats” at the VIth European Federation for Primatology Congress held in Rome in August 2015, inviting presentations from researchers studying human–primate interactions. In response to the interest shown during the symposium, Joanna M. Setchell, editor-in-chief of the International Journal of Primatology, invited us to guest edit a Special Issue on this topic. This Special Issue presents papers that illustrate different and novel ways that primates exhibit behavioral flexibility in response to human-induced habitat changes, and how this affects the long-term sustainability of their interactions with humans. We refer to these themes more generally in this introduction as “primates in anthropogenic habitats.” To provide context to the contributions, we first review the literature to identify past and present trends in research focus in primates in anthropogenic habitats. We discuss which primates are most studied and where, what kinds of behavioral adjustments are reported, and the nature of interactions reported between primates and people, with representative examples from the literature search. Next, we introduce the contributions to this Special Issue. We conclude with reflections on the current state of research in this evolving field, and suggest future lines of inquiry for its development.
We searched the literature for publications reporting primate behavior in anthropogenic habitats using the Web of Science™ database. We searched using All Databases, which included the Web of Science core collection, MEDLINE, and BIOSIS and SciELO citation indexes, covering articles published from 1970 to December 7, 2016. We searched for full-length research articles, short communications, commentaries, and reviews, but excluded studies published as abstracts only. We used the key words primate, monkey, ape, and lemur in all searches, as well as common names, e.g., macaque, baboon, capuchin, chimpanzee, in some searches. We combined key words with relevant search terms, repeating searches using alternative or synonymous terms. Search terms that returned the greatest numbers of relevant articles were human–wildlife conflict, human–wildlife interactions, crops, crop raiding, agriculture, plantation, anthropogenic, human-dominated, tourism, provisioning, and urban.
Our criterion for inclusion was that articles include information on any of the following: 1) primate behaviors that may be regarded as adjustments to, or consequences of, living in anthropogenic habitats, and thus broadly indicative of flexibility in such environments. While behavioral adjustments included reports of differences between primates in anthropogenic habitats compared to those in less human-impacted ones, we refer to these behavioral differences as adjustments for consistency with the wider literature (Sol et al. 2013; Wong and Candolin 2015). Reported adjustments include behaviors associated with diet, i.e., feeding on exotic items, activity, ranging, social organization, and reproduction; 2) behavioral responses of primates to novel aspects of, or risks associated with, anthropogenic habitats; 3) direct interactions between primates and humans (including tourists, local people, and researchers) in anthropogenic habitats; 4) human perceptions of, attitudes toward, or beliefs about, primates; and 5) the conservation implications or likely sustainability of these interactions.
We did not consider publications reporting only general effects of human disturbance such as forest fragmentation, logging, and hunting on primate occurrence, densities, distribution, or ecology (including influences on primates’ natural diet), or articles focused solely on the ecological characteristics of human-modified habitats used by primates. Likewise, we excluded publications about primate health, population genetics, or physiology, unless these also included relevant information on behavior. We limited searches to studies of wild or free-ranging primates, excluding (ex-)captive or pet primates, but note that some “wild” or free-ranging populations included in our review—especially those at tourism or religious sites—are managed by humans to considerable extents, e.g., through food provisioning or population control.
Our searches returned 517 publications that potentially met our criteria. After examining each abstract, in most cases we consulted the full article to confirm the publication’s relevance or to establish additional details about the study. The final dataset comprised 427 publications.
Our review is not intended to be exhaustive. Contributions to edited volumes were not well represented in our searches, which returned mostly journal articles. Additional relevant studies can be found in Fa and Southwick (1988), Fuentes and Wolfe (2002), Gumert et al. (2011), Paterson and Wallis (2005), Radhakrishna et al. (2013), and Waller (2016), and in journals and newsletters published by the IUCN/SSC Primate Specialist Group, which are not indexed by Web of Science. Nevertheless, Web of Science has a wide coverage of science journals including all major animal behavior, ecology, and conservation periodicals (including the “big four” primatology journals, American Journal of Primatology, Folia Primatologica, International Journal of Primatology, and Primates). Thus, we are confident that results of our literature search are representative of the field.
Growth in Research
Which Primates and Where?
The most common anthropogenic habitat in which primates interface with humans could be broadly categorized as rural agricultural (50% of publications). These were typically mosaic landscapes with areas of natural vegetation such as forest fragments bordered by or intermixed with household farms and villages, or where protected areas border agricultural land. In 14% of publications, primates were studied in habitats including large commercial timber or agricultural plantations. Twenty percent of publications concerned primates at sites visited by tourists or religious devotees, while 15% of publications described primate behavior in urban settings such as towns and cities. These habitat categories were not mutually exclusive; for example, primate tourism sites were often in urban locales.
One species of great ape (Pan troglodytes) featured in the greatest number of publications (11% of species records; Fig. 3a). Other focal species common in the dataset include those well known for inhabiting human-dominated habitats: five macaque species (Macaca spp.), three baboon species (Papio spp.), and grivet monkeys (Chlorocebus aethiops). The prevalence of chimpanzee studies does not imply that this species is especially numerous or prospers in modified habitats in association with people—unlike some macaques, for example (Richard et al. 1989). Rather, it mostly reflects recent interest in this species’ responses to anthropogenic habitat modifications (e.g., Hockings and McLennan 2012; Krief et al. 2014; McLennan and Hockings 2014). Other primate genera that have been well studied in anthropogenic habitats are more speciose than chimpanzees (especially Macaca), with research effort spread over several species. By comparison, some other species that exploit anthropogenic environments were the focus of relatively few studies in our dataset, for example, members of Cercopithecus and Sapajus, and Erythrocebus patas.
Three genera (Macaca, Papio, and Pan) accounted for more than half of the records for individual genera (N = 420; ESM Table SII). Macaca alone accounted for one third, and included 17 focal species (Fig. 3b). Four species of Papio accounted for 13% of genus records. Alouatta spp. (howlers) and Chlorocebus spp. (including grivet and vervet monkeys) also featured relatively often in the dataset.
Socioecological adjustments—described in 21% of publications—included changes in activity, ranging and habitat use, grouping and social organization, and reproduction. For example, primates that regularly eat energy-rich agricultural crops or garbage often, but not always, travel and forage less, have smaller ranges, and spend more time resting and socializing, e.g., Chlorocebus pygerythrus (Saj et al. 1999). Crop foraging primates may exhibit flexible grouping patterns with certain age–sex classes (often adult males) most likely to participate in risky forays into agricultural fields, e.g., Cercopithecus ascanius (Baranga et al. 2012) and Pan troglodytes (Hockings et al. 2012). Habitat use, including sleeping site locations, may facilitate primates’ access to human foods, e.g., Macaca fascicularis (Brotcorne et al. 2014), but can also reflect avoidance of areas of busy human activity, e.g., Hylobates moloch (Reisland and Lambert 2016). In some publications, frequent consumption of human foods is linked to shorter interbirth intervals, earlier reproductive onset, and reduced infant mortality, e.g., Papio anubis (Higham et al. 2009; Strum 2010).
Ten percent of publications report specific behavioral responses of primates to novel risks in anthropogenic habitats, such as roads, domestic dogs and cats, and humans. Behaviors described include cryptic behavior to avoid detection, e.g., Chlorocebus tantalus (Kavanagh 1980); vigilance, e.g., Papio cynocephalus (Maples et al. 1976); group cohesion and protective behavior toward vulnerable group members, e.g., Pan troglodytes (Cibot et al. 2015; Hockings et al. 2012); choice of sleeping sites to minimize predation by domestic animals, e.g., Callithrix penicillata (Duarte and Young 2011); and aggression directed at humans and dogs, e.g., Pan troglodytes (McLennan and Hill 2010). Counter-aggression in response to threats from humans was reported at some tourist sites, e.g., Macaca mulatta (Beisner et al. 2015).
Miscellaneous behavioral adjustments (13% publications) included use of exotic trees for sleeping, e.g., Pongo pygmaeus (Ancrenaz et al. 2015); use of artificial structures such as roofs and fences for travelling or resting, e.g., Semnopithecus vetulus (Moore et al. 2010); use of human water sources for drinking (Erythrocebus patas: de Jong et al. 2008); and use of high-valued agricultural fruits as potential “commodities” (Pan troglodytes: Hockings et al. 2007). Increased intragroup aggression or harassment of human visitors for food was common in provisioned primates, e.g., Macaca sylvanus (El Alami et al. 2012) and Macaca thibetana (Zhao and Deng 1992). A further 6% of publications described general use of anthropogenic habitats by primates, for example, long-term persistence in exotic plantations or agroforestry landscapes, e.g., Alouatta pigra (Zárate et al. 2014). Nineteen percent of publications identified the behavioral or ecological flexibility (or adaptability) of focal primates as a likely factor contributing to their persistence in anthropogenic habitats, e.g., Sapajus xanthosternos (Canale et al. 2013).
People and Primates
Direct behavioral interactions between people and primates were reported in 23% of publications, many concerning interactions that can be regarded as negative. Descriptions of interactions occurred disproportionally in studies of provisioned primates or primates in urban settings (56% of publications reporting direct interactions), and centered mostly on the acquisition of human food by primates, e.g., Chlorocebus aethiops (Brennan et al. 1985). Reported interactions in agricultural settings revolved mostly around protection of crops, including observations of farmers chasing or throwing objects to deter primates, e.g., Papio anubis (Warren et al. 2011).
Thirty-three percent of publications in our dataset overtly emphasized negative or competitive aspects of people–primate interactions, through use of terms such as conflict, killing, pest, and damage. Conversely, only 7% explicitly emphasized positive, peaceful, or neutral interactions, e.g., Callithrix penicillata (Leite et al. 2011); these were reported mostly in the context of human cultural attitudes that serve to protect or promote tolerance of primates, and hence allow for more sustainable interactions, e.g., Macaca tonkeana and M. ochreata (Riley and Priston 2010). Most such publications discussed both positive and negative aspects of coexistence, with local people expressing tolerance of primates in addition to concerns over crop losses or aggression from primates, e.g., Pan troglodytes (McLennan and Hill 2012).
In summary, our review confirms that primate behavior and interactions with people in anthropogenic habitats are major topics of inquiry in primatology today. Most species that were prominent in publications are classified as Least Concern in the IUCN Red List, although chimpanzees are an exception (ESM Table SI). Least Concern primates are often generalists that can fare well in landscapes dominated by human activities, e.g., some macaques and baboons. Examples of flexible behavior concerned a diversity of primates, however, including highly threatened and so-called specialist species (Nowak and Lee 2013). Nevertheless, the majority of primate species were not represented in any publications in our dataset, e.g., members of the Cheirogaleidae, Galagidae, Lepilemuridae, and Pitheciidae, which may be because they are less likely to occur in human-modified environments—perhaps owing to a lack of flexibility—or are understudied generally, or both. Evident from our review is the predominant focus on negative, i.e., conflict, compared to positive (coexistence) aspects of people–primate interactions. Although studies often provided recommendations to reduce conflict, few included an in-depth exploration of mechanisms that could enable sustainable human–primate coexistence in the long term.
Contributions to This Special Issue
As our literature review revealed, feeding on exotic plants is a primary behavioral adjustment of primates in modified habitats, and many contributions to this Special Issue concern aspects of this dietary adjustment. McLennan and Ganzhorn (2017) evaluate the common assumption that crops offer high nutritional returns compared to wild forage for primates by comparing the chemical content of wild and cultivated foods in the diet of eastern chimpanzees (Pan troglodytes schweinfurthii). Wimberger et al. (2017) examine the role of exotic plants in the feeding ecology of samango monkeys (Cercopithecus albogularis labiatus) in a matrix of residential gardens and native forest. Hockings et al. (2017) explore seed dispersal in a novel anthropogenic context, by studying patterns of dispersal of a cultivated crop (cacao, Theobroma cacao) by western chimpanzees (P. t. verus). Nowak et al. (2017) take an experimental approach to examine risk-sensitive foraging in samango monkeys (C. a. labiatus) in a habitat matrix of indigenous forest and residential gardens, where food acquisition was most risky. Schweitzer et al. (2017) examine individual participation, decision making, and collective movements by chacma baboons (Papio ursinus) when foraging on crops along the periphery of a National Park.
Three research articles use multidisciplinary methods to study human–primate interactions. Zak and Riley (2017) compared camera trap footage of crop foraging by moor macaques (Macaca maura) with farmer perceptions of macaque behavior on farms gleaned from semistructured interviews. Spagnoletti et al. (2017) combined interviews with local people with observations of crop foraging in bearded capuchins (Sapajus libidinosus) and other vertebrates using experimental plots established with the participation of local farmers. Chaves and Bicca-Marques (2017) examined crop foraging and its potential economic costs by brown howlers (Alouatta guariba clamitans), combined with interviews to understand landowners’ perceptions of this issue. Despite significant crop losses to primates, farmers in these latter two studies did not perceive losses as problematic. These examples remind us that the extent of primate crop damage does not necessarily equate to the resulting level of conflict (Hockings 2016), and that human perceptions of primates that influence tolerance of them vary in time and space (Hill and Webber 2010).
Several contributions consider how primates adjust their behavior to landscape characteristics in anthropogenic habitats. Bryson-Morrison et al. (2017) examined the activity budgets of Pan troglodytes verus in a mosaic habitat to examine the influence that risky parts of their home range—cultivated fields, roads and paths— have on their foraging behavior. Nekaris et al. (2017) studied the behavior of Javan slow lorises (Nycticebus javanicus) in response to the introduction of a cash crop, chayote, finding that the bamboo frames used to support chayote provided lorises with a novel substrate network for foraging and traveling. McCarthy et al. (2017) adopt a landscape-level approach to reveal how P. t. schweinfurthii respond to anthropogenic land-use changes through their use of cultivated and exotic tree plantation species for nesting. Eppley et al. (2017) assessed the ecological flexibility of two lemurids (Eulemur collaris and Hapalemur meridionalis) in a degraded habitat by comparing their use of exotic and pioneer plants. Spehar and Rayadin (2017) conducted camera trapping and nest surveys to examine habitat use by Bornean orangutans (Pongo pygmaeus morio) in a plantation forestry landscape.
Hill (2017) reviews current knowledge about primate crop foraging behavior, and highlights key areas for future research to promote human–primate coexistence in shared landscapes. Additionally, she outlines current debates over terms such as human–wildlife conflict and crop raiding, arguing that these obscure the complex nature of human–primate interactions and can exacerbate associated problems. In recognition of these debates, contributors to this issue endeavored to use neutral terminology when discussing crop feeding by primates. Finally, Setchell et al. (2017) present three case studies that demonstrate how careful integration of biological and ethnographic methods and perspectives can greatly improve our understanding of the complexities of human–primate interactions, and thus are crucial for addressing conservation challenges effectively.
Collectively, these articles illustrate recent advances in the field, including new insights on prominent themes in the literature, e.g., primate crop feeding, as well as traditional themes in behavioral ecology, e.g., seed dispersal, nutritional ecology, collective movements, and risk perception, and an emphasis on interdisciplinary methods and perspectives to study people–primate interactions such as camera traps combined with farmer interviews and ethnoprimatology approaches.
Primates have slow life histories and some human-induced changes likely occur too quickly for genetic adaptations to accrue. Given severe threats to the survival of primates globally (Estrada et al. 2017), it is critical to understand how different species respond to anthropogenic change, and the extent to which behavioral flexibility will help them survive in the face of ongoing changes. A goal of this Special Issue is to stimulate increased interest and new ideas on this topic.
As our review indicates, we still know little about how most primates respond behaviorally to humans and their activities, underscoring the need for research on additional, understudied species. Few primate field sites are wholly unaffected by human influence, providing researchers with opportunities to incorporate anthropogenic variables into studies of primate behavior (Hockings et al. 2015). A lack of flexible responses should be reported along with evidence of flexibility. Greater examination of the adaptive value of behavioral changes is needed: Do these adjustments help primates succeed in human-impacted environments or do they incite persecution from humans, potentially leading to extirpation of primate populations? To this end, long-term studies and comparisons among populations exposed to different forms and degrees of anthropogenic influence are invaluable.
We cannot hope to conserve primates without considering the wider political, socioeconomic, ecological, and cultural conditions under which coexistence with humans is possible, or not. Thus, we must be interested in people too. As emphasized by Setchell et al. (2017), this requires that primate researchers become “skilled at bridging disciplinary boundaries.” Care must be taken, however, when researching potentially controversial topics such as “conflicts” involving humans and primates to avoid misrepresenting or exacerbating problems (Hill 2015; Redpath et al. 2013). Anthropological investigations should be undertaken by researchers trained in the social sciences and with experience of the local sociopolitical environment in which they conduct their research. Human–primate interactions rarely stand alone and are usually associated with broader conservation issues. Thus, we should strive for a more holistic approach to primate conservation. This requires a shift from a predominant focus on constraints to coexistence to careful interdisciplinary research to identify appropriate mechanisms that will enable sustainable human–primate coexistence in the twenty-first century and beyond.
We thank all the authors and reviewers who contributed to this Special Issue. We thank Joanna Setchell for inviting us to guest edit this Special Issue and for her excellent feedback that helped us improve this manuscript. The authors were supported by a fellowship from the Leverhulme Trust to Matthew McLennan; a fellowship and research grants from Fundação CAPES, Brazil (#017/2012) and São Paulo Research Foundation–FAPESP, Brazil (BIOTA #2013/19219-2) to Noemi Spagnoletti; and a fellowship and research grant (IF/01128/2014) from Fundação para a Ciência e a Tecnologia, Portugal to Kimberley Hockings.
Compliance with Ethical Standards
Conflict of Interest
The authors declare no conflicts of interest or competing financial interest.
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