Primate Responses to Changing Environments in the Anthropocene

  • Urs KalbitzerEmail author
  • Colin A. Chapman
Part of the Developments in Primatology: Progress and Prospects book series (DIPR)


Most primate habitats are undergoing intense and rapid changes due to anthropogenic influences resulting in many primate populations being threatened. Habitat loss and fragmentation are already extensive; thus dispersal to unoccupied habitats is an unlikely adaptive response to these changes. Furthermore, most primates have slow life histories and long generation times, and because environmental change is occurring at an unprecedented rate, gene-based adaptations are also unlikely to evolve fast enough to offer successful responses to these changes. However, long primate life histories are linked to well-developed brains, which may allow primates to respond to environmental change through behavioural flexibility. Here we ask: What are the most common challenges of changing environments for primates and what do we know about their behavioural abilities to respond to such changes? To answer this question, we first review the most common types of habitat/landscape alterations, the extent of human-primate interactions, and the impact of climate change. Next, we evaluate how primates respond to these changes via behavioural flexibility, and using different approaches and datasets, we discuss how to investigate if these responses are beneficial with regard to population persistence. Finally, we discuss how comparisons across species, space, and time can be used to draw generalizations about primate responses to environmental change while considering their behavioural flexibility and the data derived from case studies. We demonstrate how understanding behavioural flexibility as a response to environmental change will be crucial to optimize conservation efforts by constructing informed management plans.


Conservation Comparative studies Behavioural ecology Behavioural flexibility Habitat change 

14.1 Introduction

14.1.1 The Anthropocene

Humans are dramatically changing the world. Our population has increased from 2.5 billion in 1950 to 7.4 billion in 2015 and is predicted to go up to 9.8 billion by 2050 (Fig. 14.1a; FAO 2017). This growth is associated with increasing resource use, including a dramatic increase in the number of livestock (Fig. 14.1b) and in the use of large areas for agriculture (Fig. 14.1c). Conversely, the proportion of areas with forest, including primary forest, is decreasing globally (Fig. 14.1d, e; FAO 2016).
Fig. 14.1

Indicators of the human impact on the world, globally and summarized for countries with and without primates. (a) Human population size with predicted growth until 2050. (b) Number of livestock including the most important mammalian breeds (cattle, sheep, pigs, goats, and buffaloes). (c) Percentage of agricultural area per total land area. (d) Percentage of forest area per total land area. (e) Percentage of primary forest area per total land area. Note that the scale for (d) and (e) differs from the scale of (c). Data from the FAOSTAT Database (FAO 2017). A country was considered a primate-range country if its boundaries were spatially intersecting with the global distribution of primates, which was determined using the “Terrestrial Mammals” shapefile from the IUCN Red List of Threatened Species (IUCN 2016)

Furthermore, the concentration of “greenhouse gases” has dramatically increased since the mid-nineteenth century, and these contribute significantly to increasing global temperature and associated changes in climate (IPCC 2014). It is well documented that over the last 130 years, the global climate has already warmed by approximately 0.85 °C, and the temperature increase is likely to exceed 2 °C by the end of the century (IPCC 2014; Raftery et al. 2017).

Finally, the current species extinction rate is much faster than the estimated evolutionary “background” extinction rate (Barnosky et al. 2011; Ceballos et al. 2015) and has been referred to as the “sixth mass extinction” (Ceballos et al. 2015). For example, conservative estimates suggest that the average rate of loss of vertebrate species over the last century is 100 times higher than the background rate (Ceballos et al. 2015). Beyond the extinction of entire species, populations of many species are in considerable decline (Ceballos et al. 2017).

Given the magnitude and range of anthropogenic impacts, Crutzen and Stoermer (2000) suggested that we label the current geological epoch as the “Anthropocene”. While the starting point of this epoch, and whether the Anthropocene even qualifies as a geological epoch, is hotly debated (Carey 2016), the term is commonly used to summarize humanity’s profound impact on the environment.

14.1.2 Primates in the Anthropocene

As a result of the increasing human population , anthropogenic landscape changes, and climate change, about 60% of the ~500 species of non-human primates (hereafter primates) are estimated to be threatened by extinction (Estrada et al. 2017). However, the impact of different human activities on primates varies across regions (Estrada et al. 2017; Almeida-Rocha et al. 2017), and within the same region different species may exhibit different population dynamics in response to the same changes (Chapman et al. 2000, 2010, 2018; Fedigan and Jack 2012).

The ability to make accurate and repeatedly reliable predictions about the population dynamics of species in response to current and anticipated environmental change will be central to creating effective conservation strategies. This will require a detailed understanding of environmental changes, their causes and cascading effects , and the biology of the species impacted by these changes. However, given the ongoing alterations to primate habitats and the bleak outlook for most primates (Estrada et al. 2017), there will not be enough time to evaluate comprehensively the ability of all primate species to respond. This will make extrapolations from existing datasets or those quickly gathered from lesser-known species and/or populations a necessity.

In this chapter, we review what we know about the ability of primates to respond to changing environments by addressing four questions: (1) What are the most common changes that occur in primate environments? (2) How do primates respond to environmental changes? (3) How can we best investigate the vulnerability of different primates to environmental changes considering that responses appear flexible? (4) How can long-term datasets be used to improve our understanding of primate vulnerability and, therefore, our ability to conserve primate populations? We then discuss the applicability and benefits of comparisons across species, space, and time and give an outlook for the integration of behavioural ecological studies into primate conservation.

14.2 What Are the Most Common Changes that Occur in Primate Environments?

14.2.1 Landscape Alterations in Primate Habitats

With very few exceptions, primates occur in tropical or subtropical regions (Fig. 14.2), and the human population is currently expanding faster in primate-range countries than in countries without primates (Fig. 14.1a). Associated with this greater human population increase in primate-range countries is the faster increase in the number of livestock (Fig. 14.1b) and expansion of agricultural land (Fig. 14.1c) compared to countries without primates. Furthermore, logging, mining, and construction of transportation networks, such as new roads, are rising in many tropical countries (Laurance et al. 2009, 2014; Weng et al. 2013). These landscape alterations often lead to disturbances, degradations, fragmentations, or the entire loss of forest areas, which is the primary habitat of primates (Reed and Fleagle 1995; Chapman et al. 2006; Lovett and Marshall 2006). For example, cropland in tropical countries expanded by 48,000 km2 per year between 1999 and 2008, largely at the expense of forest (Phalan et al. 2013). One estimate suggests that approximately 1 billion ha of additional agricultural land , primarily in developing countries, will be needed by 2050 to meet the demands of the growing human populations – an area larger than Canada (Laurance et al. 2014). As a result, forest cover is in considerable decline in primate-range countries, where, according to FAO data, 3.37% (or 72 of 2138 million ha) of forest cover has been lost between 2000 and 2014 (Fig. 14.1d). Primary forest, which is more important for many primates than disturbed forest (Gouveia et al. 2014; Chapman et al. 2018), only represented 32.33% of the total forest area in primate-range countries in 2014 and has decreased by 4.22% between 2010 and 2014 (Fig. 14.1e; see also Emrich et al. 2000; Wright and Muller-Landau 2006). In their most recent Global Forest Resources Assessment, the FAO (2016) estimated that the rate of global annual forest loss has decreased . However, in some important primate regions, such as Southeast Asia, the Congo basin, or the Brazilian Amazon, deforestation rates have increased in recent years (FAO 2017; Rigby and White 2017).
Fig. 14.2

Global distribution and species richness of primates. Distribution data are taken from the IUCN Red List of Threatened Species (IUCN 2016) and the map was created with the function lets.presabs from the letsR package (Vilela and Villalobos 2015) in R ver. 3.3.2 (R Core Team 2016)

14.2.2 Primate Interactions with Humans

Increases in human population size are likely to lead to more frequent interactions between primates and people in both natural and anthropogenic habitats (McLennan et al. 2017). For example, monkey temples in Asia, which are important refuges for primates in human-dominated landscapes, are visited by millions of people annually and bring people and primates in close, and largely peaceful, contact (e.g. (Jones-Engel et al. 2005; Conly and Johnston 2008). However, greater human population density can also lead to an increase in the hunting of “bushmeat” for local and commercial uses (Fa and Brown 2009). Primates are especially vulnerable to bushmeat hunting because they commonly have slow life histories, and many primates have relatively large bodies, which makes them a preferred target for hunters (Linder and Oates 2011; Chapman and Gogarten 2012; Wilkie et al. 2016). The encroachment of human settlements to remote areas is also leading to increasing conflicts between humans and primates, including “crop raiding” (Hill 2000; Marchal and Hill 2009; see below).

Furthermore, more frequent encounters between primates and humans can lead to an increase in parasite and disease transmission from humans and domestic animals to primates and vice versa (Woodford et al. 2002; Chapman et al. 2005b). Documented cases include the transmission of human respiratory paramyxoviruses , Streptococcus pneumoniae, and the cold (human rhinovirus C) to chimpanzees (Pan troglodytes; Köndgen et al. 2008, 2017; Boesch 2008; Scully et al. 2018) or the transmission of human measles to rhesus macaques (Macaca mulatta; Jones-Engel et al. 2006b). In Kenya, an emergence of bovine tuberculosis in baboons (Papio spp.) was caused by infected meat consumed by the monkeys from the dump at a tourist lodge (Sapolsky and Share 2004).

There are also numerous examples for the transmission of diseases from primates to humans, such as the transmission of Simian foamy virus from macaques (Macaca spp.) or Ebola from gorillas (Gorilla gorilla) and chimpanzees to humans (Leroy et al. 2004; Jones-Engel et al. 2005, 2008; Bermejo et al. 2006). Perhaps, the most prominent case is the spread of Simian immunodeficiency viruses (SIV) from different African primates to humans, which gave rise to the global AIDS pandemic (Hahn et al. 2000).

An example of transmission in both directions is the virus causing yellow fever, which can be transmitted by mosquitos between humans and primates (Fernandes et al. 2017). The most recent outbreak of yellow fever in Brazil has resulted in the death of several hundred humans and thousands of monkeys (Bicca-Marques et al. 2017; Fernandes et al. 2017). Diseases that can be transmitted from primates to humans bear an additional risk for primates : during the recent outbreak of yellow fever outbreak in Brazil, some people afraid of yellow fever harassed and killed primates (Bicca-Marques et al. 2017).

14.2.3 Effect of Climate Change on Primate Habitats

In comparison to the extensive effects of logging , agricultural clearing, and hunting, the impact of climate change has been previously considered to be minor, but this view has been replaced by the recognition that current climate change is having significant impacts on tropical ecosystems, primates, and biota in general, and this impact is likely to increase in the near future (Parmesan 2006; Brook et al. 2008; Dunham et al. 2011; Corlett 2012; Pacifici et al. 2017). Generally, the increase of temperature in primate habitats is predicted to be higher than the average increase in global temperature, while the predicted change in rainfall patterns depends on the region (Graham et al. 2016). For example, East Africa is predicted to receive more rainfall, while rainfall is predicted to decline in Mesoamerica (Altmann et al. 2002; Chapman et al. 2005a; Graham et al. 2016). Even today, some long-term primate studies have already documented temperature changes of over 4 °C in the last 40–50 years and change in annual rainfall of as much as 300 mm (Altmann et al. 2002; Chapman et al. 2005a).

The frequency and intensity of extreme weather events , such as floods, heavy precipitation, hurricanes (also called typhoons or cyclones), heat waves, droughts, and fires, are expected to become more frequent and intense in many regions (IPCC 2013; Diffenbaugh et al. 2017). Furthermore, much of the interannual climatic variation in the tropics is driven by El Niño Southern Oscillations (ENSOs ; Campos, Chap.  16, this volume; Dunham et al. 2011; Corlett 2012; Campos et al. 2015), and extreme “El Niños” (the warm phases of ENSOs) are expected to become more frequent, resulting in severe droughts in some areas, large amounts of rainfall in other areas, and more intense hurricanes in the Pacific (Cai et al. 2014, 2015).

Such changes in climate can have significant impacts on primate populations. For example, on Barro Colorado Island, Panama, fruiting, flowering, and leaf set were disrupted on six occasions between 1929 and 1994 when seasonal rains deviated from their typical pattern. In 1970, one such unusual rainfall event led to severe fruit crop failure and the mass mortality of howler monkeys (Alouatta palliata) and other animals (Foster 1982; Milton 1982; Wright et al. 1999; Wright and Calderón 2006). Additional extensive long-term monitoring of primate populations, climate, and phenology are needed to understand the future effect of climate change. For example, regression modelling of annual fruiting revealed solar irradiance and ENSO as the strongest predictors of fruiting in Kibale National Park, Uganda (Chapman et al. 2018). The projected changes in rainfall associated with climate change and coincident variation in cloud cover suggest that phenophase dynamics may be affected by climate change. As of yet, however, there is no clear signal as to how primate populations in Kibale will change, despite over 40 years of monitoring (Chapman et al. 2010, 2018).

14.2.4 Indirect, Synergistic, and Cascading Effects of Anthropogenic Changes on Primates

Perhaps the most significant changes in the future will be the result of various indirect, cascading, and synergistic effects on primate habitats that have not been anticipated. For example, climate change, habitat loss, and fragmentation can all affect plant phenology (Parmesan 2006; Morellato et al. 2016). This means that temporal and spatial variation in food abundance can change, potentially leading to the immigration of new competitors, predators, or pathogens into primate habitats. For example, Rothman et al. (2015) showed a general decline in the nutritional value of leaves in Kibale, Uganda, over as little as 15 years, and such changes have the potential to decrease habitat suitability for local populations of leaf-eating red colobus (Procolobus rufomitratus) and black-and-white colobus (Colobus guereza). Some environmental changes also have the potential to lead to other perturbations (i.e. cascading effects) and to amplify one another (i.e. synergistic effects; (Brook et al. 2008). For example, logging can affect primates by (1) decreasing food availability and (2) creating roads that fragment primate habitats and facilitate (3) bushmeat hunting and serve to (4) increase the opportunities for disease transmission (Chapman et al. 2005b; Goldberg et al. 2008; Remis and Jost Robinson 2012).

14.2.5 Protection and Restoration of Primate Habitats

Some disturbed primate habitats are changing because humans undertake efforts to protect and/or restore them, and such efforts can have significant benefits to primate populations (Fedigan and Jack 2001; Robbins et al. 2011; Strier and Ives 2012; Wheeler et al. 2016; Omeja et al. 2016). Ideally, these efforts will provide new protected areas or improve existing habitats and lead to viable populations of primates and other organisms. Since the 1990s, protected areas have increased in size globally, primate regions included (Butchart et al. 2010; Rands et al. 2010; Estrada et al. 2017). However, these positive developments need to be viewed realistically (Joppa et al. 2008; Andam et al. 2008; Joppa and Pfaff 2009, 2010). For example, many primates do not live inside protected areas (Meijaard et al. 2010; Estrada et al. 2017). Also, although protected areas are normally effective at protecting land from being cleared, they are less effective at eliminating logging, human-created fire , and bushmeat hunting (Oates 1996; Chapman and Peres 2001; Bruner et al. 2001; Hartter et al. 2011; Gaveau et al. 2016). Researching how to make the largest conservation gains for primates from existing and new conservation areas is a clear priority that will necessitate working closely with the local communities.

In primate-range countries, human population growth is much greater in urban than in rural areas as people move from the farms to the cities, and populations in rural areas are predicted to be on a general decline in the next few years (Fig. 14.3). With these trends, abandoned areas that were occupied by primates prior to being converted to human uses are increasing (Jacob et al. 2008). There are a variety of trajectories for these lands: they could be converted into huge agricultural monocultures, like palm oil plantations (Linder 2013), or to agroecosystems where some form of primate conservation is possible (Estrada et al. 2012), or to agricultural land with fragments and corridors (Pozo-Montuy et al. 2013; see also Meijaard et al. 2010). Alternatively, the land could be allowed to regenerate to natural forest, which offers greater potential for the persistence of primates (Chapman 2018). For example, Baya and Storch (2010) surveyed a village site in Korup National Park, Cameroon, that was abandoned 7–8 years previously, and they found that all eight species of endemic primates had repopulated the area; in addition, sighting frequency was not significantly different from other sectors of the park surveyed in 2004–2005 (Linder 2008). In Kibale National Park, Uganda, 7 years after an area of grassland was replanted with trees as part of a carbon offset programme, all species of diurnal primates were present in high numbers, including the endangered red colobus and chimpanzee (Omeja et al. 2012, 2016; Chapman et al. 2018).
Fig. 14.3

Changes in human populations size with predicted growth until 2050 for (a) urban and for (b) rural areas. Data sources are the same as for Fig. 14.1

The outcome of such conservation efforts is, however, not always predictable because other factors , such as climate and the immigration of competitors (e.g. elephants; Omeja et al. 2014, 2016), can change, and different species of primates respond in different ways to habitat regeneration (Fedigan and Jack 2001, 2012; Chapman et al. 2018).

14.3 How Do Primates Respond to Environmental Changes?

14.3.1 General Ways to Respond to Changing Environments

Animals possess three key possible ways to responding to changing environments (Wong and Candolin 2015): (1) moving to other areas that fit their requirements, i.e. dispersal; (2) evolving adaptations to the new conditions, i.e. evolutionary (or genetic) change; or (3) exhibiting behavioural responses that are already in their repertoire (or reaction norms) to cope with new conditions, i.e. phenotypic plasticity.

Habitat loss is already a major concern for the survival of primates (Estrada et al. 2017), and, therefore, unoccupied habitat with the same characteristics as the current habitat is typically nonexistent. Furthermore, fragmentation results in physical barriers between suitable patches, which increases the risks for dispersing individuals (Arroyo-Rodríguez et al. 2013). Thus, dispersal is an unlikely suitable response to the Anthropocene.

Mammalian species with slow life histories, such as many even-toed ungulates and carnivores, are assumed to be even more vulnerable to extinction than mammals with fast life histories, like most rodents (Purvis et al. 2000; Gonzalez-Voyer et al. 2016). Of course, many primates have very slow life histories: on average, females give birth for the first time around 4 years of age (ranging from 256 days to 13.9 years), inter-birth intervals are commonly longer than a year (mean = 1.5 years, range = 0.4–5.5 years), and, with the exception of very few species, females give birth to only a single infant per birth (values based on data from the PanTHERIA database1; Jones et al. 2009). Most anthropogenic changes, however, occur very rapidly, and for primates and other long-lived animals, it is very unlikely that evolutionary changes are able to keep pace with these changes (Wong and Candolin 2015).

However, primates have relatively large brains, and it has been suggested that large brains are associated with higher behavioural flexibility, conferring advantages in dealing with both social and ecological challenges (Strier, Chap.  2, this volume; Reader and Laland 2002; Sol et al. 2008). Thus, given the constraints on dispersal and evolutionary change as a response to environmental change, behavioural adjustments appear to be the most likely possibility with which primates might respond to the Anthropocene. What kind of flexible, behavioural responses can primates exhibit to cope with the anthropogenic environmental changes thus becomes a critical question that must be answered to inform conservation strategies.

14.3.2 Primate Behavioural Responses to Landscape Alterations

In response to habitat fragmentations , disturbances, or degradations, primates can change their ranging patterns, activity budgets, and diet (Wong et al. 2006; Wong and Sicotte 2007; Pebsworth et al. 2012; Mekonnen et al. 2017; McLennan et al. 2017). Furthermore, the spatial and temporal distribution of food resources is considered to be one of the most important factors affecting social behaviour and mating patterns (i.e. primate socioecological theory; Wrangham 1980; Isbell 1991; Sterck et al. 1997; Snaith and Chapman 2007; Koenig et al. 2013). Thus, if human impact on primate habitats affects the abundance and distribution of their food resources changes in group size and composition, reproductive patterns or social relationships may occur (langurs, Sterck 1999; tana river colobus, Cercocebus galeritus, Mbora et al. 2009; red colobus, Gogarten et al. 2015; muriquis, Brachyteles hypoxanthus, Strier and Mendes 2012).

Some of these behavioural responses allow primates to survive in human-modified landscapes (Schwitzer et al. 2011; Bonilla-Sánchez et al. 2012; Chapman et al. 2016; McLennan et al. 2017), such as tree plantations or suburban settings (Moore et al. 2010; Hoffman and O’Riain 2011). In some cases, primates even thrive in human-modified landscapes by supplementing their natural diet with human-cultivated resources via crop feeding (Hill 2000; Marchal and Hill 2009; Chapman et al. 2016); feeding on garbage, food items in houses, or fruit trees in gardens (Hoffman and O’Riain 2012); or being voluntarily provisioned with food from humans. For example, some primates obtain large parts of their diet from local people and tourists at monkey temples in Asia (Jones-Engel et al. 2005; Fuentes and Gamerl 2005).

14.3.3 Primate Behavioural Responses to Interactions with Humans

Where humans do not pose a threat to them, primates can easily habituate to humans. For example, the ursine colobus (Colobus vellerosus) at the Boabeng-Fiema Monkey Sanctuary in Ghana (Wong et al. 2006), different macaque species at monkey temples in Asia (Fuentes and Gamerl 2005; Jones-Engel et al. 2006a), and baboons close to tourist lodges and human settlements in Senegal or Botswana (UK, personal observation) are all examples where primates peacefully coexist with humans, and, in some cases, this coexistence can even result in economic benefits to local human populations (Fuentes and Gamerl 2005). However, if encounters are less peaceful, such as occurs in the context of bushmeat hunting, primates can become more cryptic, vigilant, try to avoid risky areas, and become more aggressive towards humans and dogs (Remis and Jost Robinson 2012; McLennan et al. 2017). For example, vervets (Chlorocebus tantalus) in areas of Cameroon where they were heavily hunted by humans with dogs suppress loud, conspicuous alarm calls directed at dogs , possibly to avoid detection (Kavanagh 1980).

14.3.4 Primate Behavioural Responses to Climate Change

In response to increasing temperatures , which can make metabolic costs of moving or foraging unsustainable during the hottest time of the day, primates can change their daily activity patterns. For example, they may rest or socialize in the shade during the middle of the day and spend more time foraging during cooler periods (Hill 2005). Primates also show a high degree of variability in birth seasonality, ranging from strictly seasonal breeding species, such as macaques, to species in which females can give birth throughout the year, such as baboons (Papio spp.; Janson and Verdolin 2005). In such flexible species, females may adjust their breeding behaviour by only reproducing during favourable times. For example, yellow baboons in Kenya (P. cynocephalus) breed throughout the year, but females are less likely to cycle or to conceive after periods of extreme heat (Beehner et al. 2006). However, how quickly a population modifies their seasonal reproductive patterns remains to be determined.

While some primates rarely drink water, other species need year-round access to water sources (Hill 2005; McDougall et al. 2010; Fedigan and Jack 2012). If the habitat of these obligate drinkers receives less rainfall, water sources can become rare and widely dispersed, requiring changes in ranging patterns in order to maintain access to drinking water, as has been documented for vervet monkeys (Chlorocebus aethiops; McDougall et al. 2010). Such shifts could become permanent if previously favourable areas become unsuitable year-round. This may increase encounters between groups, leading to higher energy expenditures, increased stress, and even elevated mortality levels. In contrast, more rainfall and shorter dry periods may have no direct, but rather indirect, effects on primates, such as causing temporal shifts of food availability, or fruit crop failure, which has been documented to cause increased mortality (Milton 1982; Wright et al. 1999; Wright and Calderón 2006).

Hurricanes represent another extreme weather event with potentially severe impact on primates and their habitats that may increase in frequency and intensity with climate change (Erhart and Overdorff 2008; Dunham et al. 2011; Johnson et al. 2011; Schaffner et al. 2012). Primates respond in various ways to the impact of hurricanes. For example, black howlers (Alouatta pigra) and spider monkeys (Ateles geoffroyi) in Belize and toque macaques (Macaca sinica) in Sri Lanka responded to the habitat destruction following hurricanes by changes in activity budgets, diet, and social behaviour (Behie et al. in press; Dittus 1988; Behie and Pavelka 2005, 2013).

14.3.5 Primate Behavioural Responses to Indirect and Synergistic Effects of Changing Environments

Changes in plant phenology may represent one of the most important indirect effects of anthropogenic activities on primates because it can lead to a change in temporal and spatial distribution of food resources. As discussed above, primates can respond to such alterations by adjusting group size, social structure, and mating patterns. Furthermore, they can shift their diets and rely on fallback food when their preferred resources become scarce during some (or all) periods of the year (Hanya and Chapman 2012). Temporal variation in food abundance is also one of the main factors suspected to determine timing of reproduction (Janson and Verdolin 2005; Carnegie et al. 2011). For example, capuchin monkeys in Santa Rosa can give birth throughout the year but do so mostly during the period of highest fruit abundance (Carnegie et al. 2011). Thus, if temporal variation in food availability changes, some primates may shift their birth peak. Cascading and synergistic effects describe processes rather than specific types of environmental change; thus, primate responses will depend on the nature of the changes involved in such processes (e.g. habitat fragmentation, hunting), which, to a large extent, are unknown.

14.4 How Can We Best Investigate the Vulnerability of Different Primates to Environmental Changes Considering that Responses Appear Flexible?

Primates show highly flexible behaviour which they can adjust to various types of environmental change, but are these behavioural responses beneficial and sufficient to ensure their survival? And why are some species doing well in human-dominated landscapes, while other species already have gone extinct2 or are threatened by extinction?

There are three general approaches to investigating the vulnerability of primates to anthropogenic change: (1) comparative studies of different populations and species, (2) niche modelling studies, and (3) behavioural ecological studies based on the behaviour of individuals.

14.4.1 Comparative Studies

Studies using the comparative method commonly aim to investigate the relationships among morphological, life history, behavioural, and ecological variables across species while controlling for the effects associated with phylogenetic relatedness (Harvey and Pagel 1991; Nunn and Barton 2001). With regard to species or population persistence, such analyses aspire to understand the relationships among biological variables (e.g. body weight, age at first reproduction) and variables reflecting the vulnerability of species to extinction. Using this approach, Purvis et al. (2000) showed that primates with small geographic distributions, large body mass, and low population density are at higher risk of extinction than are species with large distribution, small body mass, and high population density. Furthermore, mammalian species that are highly specialized with regard to diet or habitat are more threatened by habitat changes, while species with slow life histories, such as primates, are more threatened by hunting and other direct effects (González-Suárez et al. 2013).

The notion that behavioural flexibility may be beneficial for coping with environmental change has received support from a comparative study showing that within-species variability in life history (e.g. age at first reproduction) and population density appears to reduce the vulnerability of mammals to extinction (González-Suárez and Revilla 2013). Furthermore, mammals with relatively large brains (and therefore presumably greater behavioural flexibility) are more successful in novel environments than mammals with relatively small brains (Sol et al. 2008). However, a different study indicated that larger brains in primates and other mammals are associated with increased vulnerability to extinction (Gonzalez-Voyer et al. 2016). Thus, the behavioural flexibility resulting from large brains in primates may not outweigh the costs of slow life histories and the higher energy demands that large brains necessitate and, therefore, may even represent a disadvantage in this heavily human-dominated world.

Phylogenetic comparative studies require large datasets (e.g. PanTHERIA or AnAge; Jones et al. 2009; Tacutu et al. 2013), but there are often problems related to accuracy and comparability (Borries et al. 2016). Furthermore, animals are constantly making behavioural adjustments to environmental conditions, and, therefore, species parameters, such as group size, vary considerably depending on the study location, the provisioning of the group, or the study period (Strier 2009, 2017; Borries et al. 2016). To address this concern, some studies include the coefficient of variation (CV) of a variable to explicitly assess the effect of within-species variation (González-Suárez and Revilla 2013; Kamilar and Baden 2014). However, to observe a large proportion of the possible variation within a species, samples from long periods of time and different locations are necessary (Chapman et al., Chap.  17, this volume; Hogan and Melin, Chap.  10, this volume), and for most species this is simply not available. In such analyses it is also important to consider that variation assessed by CVs is positively related to the number of data points and the duration of the study (Strier, Chap.  2, this volume; González-Suárez and Revilla 2013; Strier et al. 2014). Finally, comparative studies are limited to the variables included in comparative databases, and these may not necessarily be the variables of interest with regard to the survival of a population.

Thus, while comparative studies can lead to important insights and generalizations as to how different species or populations of primates may or may not respond to anthropogenic changes, these limitations should be kept in mind, and it will remain important to investigate single species as this information is “essential to understand the species-specific aspects of vulnerability and potential for recovery” (Fedigan and Jack 2012, p. 181).

14.4.2 Niche Modelling Studies

One approach to assessing vulnerability at the species level is through niche modelling (e.g. Johnson and Brown, Chap.  15, this volume) which investigates broader factors (e.g. rainfall patterns, elevation, temperature) that affect the geographical distribution of a species. By extrapolating from the results of such studies, it is possible to predict which unoccupied habitats might be suitable for a specific species (Vidal-García and Serio-Silva 2011) and how this species might be able to cope with anticipated environmental change in their current habitats.

For example, Vidal-Garcia and Serio-Silva (2011) used a niche modelling approach to develop a distribution model for the primates of Southern Mexico. Using records of the presence of the 3 endemic primates and 19 potential environmental predictors of their distribution, they found strong relationships (e.g. Alouatta palliata was strongly associated with precipitation during the coldest quarter of the year). By using this modelling approach, these authors located areas with a high probability of the presence of the target primate, information that is now being used in conservation planning. However, such studies do not typically have the data required to investigate the proximate causes limiting population distributions, such as daily access to drinking water sources or required plant resources.

14.4.3 Behavioural Ecological Approach

Investigating the mechanisms underlying the persistence or extinction of populations on the individual level can be achieved by combining behavioural ecology with conservation biology. This behavioural ecological approach to conservation has also been labelled as “Conservation Behaviour” (Caro and Durant 1995; Blumstein and Fernández-Juricic 2010; Blumstein 2012), and it can contribute to many critical aspects of conservation, including predictions of population persistence, design of protected reserves, and management of populations (Caro and Durant 1995).

The idea behind conservation behaviour is that individual behavioural responses to environmental changes determine individual survival, reproduction, and migration, which ultimately determines population dynamics (Blumstein 2012; Wong and Candolin 2015). In other words, the focus on individual survival and reproduction of behavioural ecological studies is shifted to a focus on the broader survival of populations in conservation behaviour. Blumstein (2012) stressed the importance of social and mating behaviour in such investigations, as the link from environmental variation to demographic success often goes through social structure and breeding system. For example, environmental factors affect dispersal and mating patterns, which determine effective, and, therefore, minimal viable population sizes (Caro and Durant 1995). Knowing these parameters is important when designing protected areas of the appropriate size, shape, and connectivity. Anthropogenic changes can also affect the occurrence of sexually selected behaviours, such as male infanticide in primates, which can impede population growth (Jack and Fedigan, Chap.  6, this volume; Sterck 1999). Thus, environmental conditions such as the distribution and abundance of resources, predator density, cover from predators, and pathogens are linked to demographic structure through individual behaviour. Investigating this link can reveal insights into the adaptiveness of primate behavioural flexibility, uncover key factors that determine population persistence , and predict population responses to anthropogenic change, all of which can help improve conservation efforts.

14.5 How Can Long-Term Datasets Be Used to Improve Our Understanding of Primate Vulnerability and, Therefore, Our Ability to Conserve Primate Populations?

As a result of the slow life histories of primates, long-term datasets spanning several generations are often necessary to observe the relationship between environmental change and population dynamics (Strier 2009; Fedigan and Jack 2012; Campos et al. 2015; Chapman et al. 2018). Such datasets require a lot of effort and dedication to collect; thus only a few primate populations have now been continuously observed for the needed duration (e.g. the seven populations of different primate species that are part of the “Primate Life History Database”; see Strier et al. 2010; Campos et al. 2017). The collection of such long-term data also requires substantial continuous funding, a requirement that is getting harder to achieve despite a very apparent need.

Long-term data can be supplemented from other sources to generate more comprehensive datasets with which to investigate the impact of environmental change on population dynamics. To assess environmental change, questionnaires can be used to assess human activity and its impact on primates and their habitats (McKinney 2015). Aerial photographs and historic and contemporary satellite imagery can reveal information about changes in forest structure and coverage (Harper et al. 2007). Satellite imagery can also be used to estimate human-primate interactions by assessing human population density and the distance between human settlements and roads (e.g. logging routes) to primate habitats (Espinosa et al. 2014). Long-term data on past, current, and predicted temperature or rainfall are available from online resources, such as WorldClim (, or from the Data Distribution Centre of the Intergovernmental Panel on Climate Change (IPCC DDC ; Some long-term datasets also include plant phenology data (e.g. Santa Rosa, Costa Rica, Hogan and Melin, Chap.  10, this volume; Kibale, Uganda, Chapman et al. 2018; Cabang Panti Research Station, Borneo, Dillis et al. 2015), which, in combination with plant transects and food lists, can be used to assess variation in food availability over space and time.

Data on individual behaviour is often the central piece of long-term primate behavioural ecological studies and can be used to assess changes in both activity budgets and more specific patterns of social, feeding, and ranging behaviour in response to environmental change. Furthermore, long-term studies also put a great deal of effort into collecting data on life-history events such as emigration, death, or birth of individuals. These data are essential to assess the effect of individual behaviour on survival and reproduction, which is of central interest to behavioural ecologists. The same long-term life-history data can also be used to assess the effects of environmental change on survival and fertility rates (Campos et al. 2017). However, to assess changes in demographic structure of an entire population, regular area-wide censuses are necessary (e.g. Barro Colorado Island, Panama, Milton and Giacalone 2014; Beza Mahafaly, Sussman et al. 2012; Hacienda La Pacifica, Costa Rica, Clarke and Glander 2010; Hato Masaguaral, Venezuela, Rudran and Fernandez-Duque 2003; Kibale, Uganda, Chapman et al. 2018; Kinkazan, Japan, Yamagiwa 2010; Santa Rosa, Costa Rica, Fedigan and Jack 2012) ideally including knowledge about sex and age composition of individuals in the encountered groups. Ultimately, changes in demographic structure can be used to make predictions about the survival of populations .

Such comprehensive datasets can be used to investigate how primates respond to changing environments, to make predictions about the viability of populations, and to implement conservation measures. For example, if females can breed throughout the year, how does this affect individual fitness and the dynamics within the population? Such questions can be addressed by using a comprehensive, longitudinal dataset to (1) assess fluctuation in food availability, temperature, and rainfall patterns; (2) determine the timing of life-history events with regard to environmental conditions for the entire populations; (3) investigate whether individuals have greater reproductive success, better health, and longer life expectancy if they adjust the timing of life-history events from year to year according to environmental conditions; and finally (4) assess how this individual flexibility affects the demographic structures of the entire population and improves the population viability in comparison to non-flexible species (see also Campos et al. 2017; Strier, Chap.  2, this volume). If flexibility is adaptive, these populations should be less affected by periods of unfavourable conditions, such as periods of resource scarcity. The knowledge acquired could be used to either provision susceptible populations with water or food during crucial periods (but this creates issues as well; e.g. Asquith 1989) or to specifically design protected areas that ensure sufficient resources and protection during these periods.

Building comprehensive and meaningful species models that are generalizable to a variety of habitats that link environmental change to population persistence through individual behaviour is challenging and currently only possible for very few primate species. Nevertheless, investigating the link between only some of the factors at a time, for example, the consequence of changes in temperature and rainfall on demography (Campos et al. 2015) or the fluctuation in resource availability or logging on population abundance (Chapman et al. 2018), can also be informative with regard to understanding primate adaptations to changing environments. Importantly, based on such studies, researchers could go back to their datasets and ask more specific questions about the behavioural mechanisms underlying the observed link (Fedigan and Jack 2001, 2012).

14.6 Comparisons Across Species, Space, and Time

While a single-species approach is necessary to identify the mechanism underlying primate population responses to environmental change, responding to major issues like climate change, deforestation, or bushmeat requires generalizations that are applicable to sets of species (phylogenetic and functional groups), times, and locations. Environmental factors, individual behaviour, and the demographic structure of populations can be compared along three different dimensions to disentangle flexibility and phylogenetic constraints in primate responses to changing environments (Chapman and Rothman 2009). First, long-term studies on a single population can be considered to be a comparative study over time (temporal dimension) because a population at one given time is compared with the same population at another time when conditions have changed. Second, populations of the same species can be compared across different habitats (spatial dimension). Third, different species can be compared within the same habitat (phylogenetic dimension). Furthermore, these three dimensions can be combined, for example, by comparing different species across different habitats (i.e. spatial and phylogenetic dimension). When investigating responses to environmental change, we think that the following three types of comparisons as especially useful: (1) spatial comparisons, (2) phylogenetic and temporal comparisons, and (3) phylogenetic, spatial, and temporal comparisons.

14.6.1 Spatial Comparisons

Comparisons within the same species across different habitats that have experienced different types and degrees of modification can advance our understanding of the potential of within-species flexibility (Struhsaker 1999; Chapman and Peres 2001; Chapman et al. 2010). For example, Meijaard et al. (2010) found that population densities of Bornean orangutans between conservation areas and pulp and paper plantations were similar and suggested that behavioural flexibility facilitated these apes surviving in modified landscapes. Such contrasts can be considered natural experiments that allow us to study animal adaptions (Schroeder et al. 2011; but see Caro and Sherman 2011 for limitations of this approach).

14.6.2 Phylogenetic and Temporal Comparisons

By comparing different species in the same habitat over time, it is possible to directly compare responses across species towards the same environmental changes. For example, howler and capuchin monkeys (Cebus capucinus imitator) in Santa Rosa, Costa Rica, showed differences in population growth in the same regenerating forest. In this case, both species faced the same changes in the environment, and differences in population dynamics can probably be attributed to differences in diet, life-history pace, dispersal patterns, and behavioural flexibility (Fedigan and Jack 2001, 2012). Additionally, studying several species within the same habitat enables the investigation of interactive effects at the community level, such as density compensation (Peres and Dolman 2000).

14.6.3 Phylogenetic, Spatial, and Temporal Comparisons

Comparisons of different species across different locations over time can be insightful if the locations are undergoing similar changes. For example, Campos et al. (2017) analysed long-term data to investigate the impact of climate variability on fertility and survival rates in seven species of primates and found out that highly seasonal species appear to be more vulnerable to climate change than non-seasonally breeding species. The challenge of such comparisons is to control for ecological and demographic differences between locations that potentially affect the observed response (Strier 2009), such as the number of receptive females when comparing male behaviour across species and habitats (e.g. Kalbitzer et al. 2015).

14.7 Integrating Behavioural Ecological Studies into Primate Conservation

The integration of conservation biology and behavioural ecology faces many challenges (Caro and Sherman 2013), yet a better incorporation of these two theoretical frameworks could help to improve efforts to protect primates. Primate behavioural ecologists can help to improve this integration by specifically considering (1) the effects of anthropogenic changes on behaviour and (2) the effects of specific behavioural responses, for example, the alteration of breeding seasonality, on population dynamics (McLennan et al. 2017). It is also important to make relevant data more easily available to other conservation biologists, managers, and the public. Similar to some conservation-oriented journals (e.g. Biological Conservation), behavioural ecological journals could include a dedicated space at the end of their published articles in which authors are asked to include information on the relevance, if any, of their findings to conservation. This could include information on predicted changes in population size as a result of environmental change or a description of the size and quality of habitat necessary to preserve the future populations. Furthermore, determining and communicating possible key factors that limit population growth or increase mortality in its current habitat, such as a lack of drinking water or protein-rich food (Milton and Giacalone 2014), may be critical to the implementation of measures, such as the artificial provisioning of these resources , or to guide regeneration projects that ensure the viability of these populations despite anticipated environmental change.

14.8 Conclusion

Our world is undergoing anthropogenic changes at an unprecedented pace and scale; thus it is crucial to understand how primates respond to these changes to prevent further extinctions. Behavioural flexibility will be vital for many primates to survive, and careful comparative investigations using data spanning generations of primates are required to determine whether this flexibility is sufficient to prevent population decline and to improve conservation efforts. Fortunately, some ongoing long-term studies have already collected data over a few decades, which can be supplemented with available data on environmental change to conduct analyses as to how primates are able to respond to the Anthropocene. However, based on the finding of the current long-term studies that are just now emerging, we highlight the need for more long-term studies that are explicitly designed to quantify change in behaviours and identify potential drivers of changes. For the many primate species without longitudinal data, extrapolating from other long-term studies offers the potential to obtain valuable conservation insights.

While it is important and often exciting to investigate questions about the ability of organisms to respond to environmental change, we should also make use of our own potential for flexibility and modify our own behaviour to preserve the exciting diversity of primates and biodiversity that we find in this world.


  1. 1.

    The calculation of age of first birth includes data from 102 primate species, and the calculation of inter-birth intervals included data from 108 primate species. These averages are not corrected for phylogenetic relatedness and might be biased depending on the inclusion of varying number of primates from different taxonomic groups.

  2. 2.

    It seems almost a certainty that with the disappearance of Miss Waldron’s red colobus (Procolobus waldroni), the first primate species has been driven to extinction in modern times (McGraw 2005; Oates et al. 2016).



Most importantly, we want to thank Linda Fedigan for her inspiring research and the great collaboration during the last 3+ years (UK) and for the last 40+ years (CAC) and for giving us a good reason to having a great symposium in honour of her academic career (Jack and Kalbitzer 2017). Our motivation for this chapter came from our work in different primate habitats across the globe and the observation that some species are very successful in dealing with human pressures, while others disappear. Furthermore, UK is grateful that he had the opportunity to work with the PACE database at the University of Calgary for the last few years, which was very inspiring regarding the discovery of the potential lying in such datasets. We also thank Katharine Jack, Peter Henzi, and one anonymous reviewer for providing us with constructive feedback on earlier drafts of this manuscript. UK was funded by an Eyes High Postdoctoral Fellowship from the University of Calgary while writing this manuscript.


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© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Department of Anthropology and ArchaeologyUniversity of CalgaryCalgaryCanada
  2. 2.Department of Anthropology and McGill School of EnvironmentMcGill UniversityMontrealCanada
  3. 3.Makerere University Biological Field StationFort PortalUganda
  4. 4.Wildlife Conservation SocietyBronxUSA
  5. 5.Section of Social Systems Evolution, Primate Research InstituteKyoto UniversityKyotoJapan

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