Around the world, as the climate begins to change, so too does the primate genus, Macaca. Macaca, or macaques, are a very successful primate because of their generalized “plastic” behaviors which refers to their abilities to exploit the habitat around them for their own benefit. Although many primates are known for being opportunistic generalizers, not all of them are as plastic as macaques. Macaques range in a variety of places depending on food availability from urban Hindi shrines with humans to high, montane forests outside of human reach. Even in a world which is changing due to human influences, macaques are able to shift along and take advantage of the opportunities humans have presented. As a genus, macaques are able to face changing ecological and demographic circumstances because of their plastic characteristics in response to food availability by adjusting their dietary, social and ranging behavioral strategies.
Rhesus macaques (Macaca mulatta) near a temple in Agra, northern India. (Photo by: Thomas Schoch, WikiMedia Commons)
Macaques are considered plastic largely in part because of their ability to fall back on other strategies when circumstances become such that where the benefits of changing would outweigh the cost of specializing. In many cases, the deciding characteristic of manipulate behavior to exploit the geographic range depends on the strategies enabled related to food resources. Food resources are at the core of the adjustments to behavioral strategies in macaques which can lead to interspecies variation in strategies with regards to size of populations, home ranges, and dietary preferences. Behavioral strategies can also vary between populations due to geographic differences as well. While food resources largely determine many facets about macaque behavioral strategies, it largely depends on the availability of preferred foods in a given home range on how macaques tend to respond.
Food: the plastic crux
Macaques, like many other primates, have a complex dietary system. Overall, macaques tend to prefer fruits but will also consume seeds, leaves, buds, roots, flowers, herbs, invertebrates, grain, bark, and moss (Menard 2004). Most macaques are non-specialized, allowing for consumption of a wide variety of available food resources as opposed to relying only on specific foods like leaves as some colobines. By being able to generalize and take advantage of these resources, macaques are able to respond to shortages of their preferred foods by falling back on lower quality foods such as leaves and herbs. However, this plasticity is dependent on a matter of issues.
As with every living creature, macaques’ food resources are heavily dependent upon geographic range and climatic conditions within the range. Given that macaques have been known to range from Morocco to northern Japan, there are variations on the dietary preferences of macaque species based on where each macaque population is situated. Macaques which reside in colder climates such as Arunachal macaques (Macaca munzala) and Japanese macaques (M. fuscata), these species tend to rely heavily on bark and other mature leaves in winter seasons (Mendiratta 2009). These species fall back on these high-fiber foods and exploit their generalizing abilities in order to live in these habitats during these seasons and avoid competition. While, in rhesus macaques (M. mulatta) which reside in Himalayan foothills are primarily folivorous; others which reside in more southern geographical ranges often prefer fruits and agricultural crops for subsistence as a higher-quality food to sustain them through more temperate regions (Richard et al. 1989; Fooden 2000). Rhesus monkeys that live in different geographical ranges and climates tend to have different dietary strategies as per the plastic nature of macaques. Although strategies may change depending on geographical range and climate, humans also have a significant role in determining some of the strategies as well.
A pig-tailed macaque (Macaca nemestrina) chowing down. (Photo by: BBC factfiles)
Humans have been responsible for multiple feeding strategy shifts by macaques to adjust to anthropogenic pressures such as deforestation. Deforestation has removed valuable habitats from macaques and is the primary threat all macaques face (Riley and Priston 2010). For example, crested black macaques (M. nigra) found in disturbed habitats consume more insects than those in less disturbed areas (Riley 2007). Insects are an abundant food source in these fragmented habitats as pools of water form where trees were; these pools often serve as an ideal reservoir for larvae. When these forests are fragmented, insect populations increase from the greater potential for reservoirs. As a result, macaques have adjusted to this shift in changing food resources by utilizing a plastic feeding behavioral response to a shifting climate within their habitat.
Plastic social behavioral ecology
A pair of captive Japanese macaques (Macaca fuscata) at the Milwaukee Zoo; the female is grooming the male. (Photo by: A.V.S.)
Overall, social behaviors are largely dependent upon food resources and accounts for species-specific variations in population size, mating seasons, and ranging patterns. Macaques in the wild typically live in bisexual, multi-male and multi-female groups of generally between 15 and 50 individuals, but group sizes can expand to 90 individuals in cases where provisioning occurs (Fooden 1986; Menard 2004). Typically, macaques have large overall populations and fission off into smaller subgroups in order to forage more effectively and reduce competition within group members. In situations where humans are provisioning macaques, there is less reason to fission into smaller subgroups as food can be found more easily; therefore, many macaques stick together in larger groups. Conversely, in the wild, where food is more scattered, macaques resort to other foraging strategies aside from fissioning to obtain resources that determines other factors related to sociality within groups.
For macaques, mating seasons are highly plastic because of an adaptation to the climate in ranges and on the quality of food availability during those times. Species in tropical regions, such as stumptailed macaques (M. arctoides) have year round breeding periods in which individuals are born every month (Smith 1984). Whereas, species which live in temperate regions such as Assamese macaques (M. assamensis) have seasonal births from April to July during the rainy season when food is more abundant (Furtbauer et al. 2010). Given that both of these species have variations in resource availability based on the seasonal time of year, these macaques display the overall plastic tendencies of the genus by adapting to climates effectively by exploiting time when food is plentiful enough to ensure the mother’s nutritional requirements are met as a result of the cost of reproduction.
The availability of food not only determines the size of groups and reproductive seasonality, but also the plasticity of demographic sex ratio of offspring through hierarchy. In toque and pig-tailed (M. nemestrina) macaques, higher-ranking females which were larger and healthier were more likely to give birth to female offspring, whereas smaller, and less healthy lower-ranking females gave birth to more male offspring (Dittus 1998; Maestripieri 2002). For these situations, higher-ranking females are able to have a priority-of-access to higher-quality foods that, in turn, may play a role in the ability to have females compared to lower-ranking females. These lower-ranking females often have to compete for or concede higher-quality food resources to higher-ranking individuals at the expense of their own nutritional requirements; a reflection of female adiposity. Interestingly enough, female rhesus macaques display the demographic characteristic differently; instead of higher-ranking females giving birth to more female offspring, middle-ranking females in Cayo Santiago were the most likely to give birth to female offspring (Berman 1988). It is thought that because rhesus macaques on this island are provisioned, variation of competitive abilities are reduced, removing the relationship of hierarchy, rank, and female adiposity conditions in this circumstance as per adjustment from settings in nature where food is patchy as opposed to provisioned. As a result, food availability plays a significant role in the plasticity of social behaviors in terms of group size, breeding periods, and also demographic sex ratio.
Plastic home on the range
The biogeographic range of the genus, Macaca. (Image from: theodora.com/maps)
In order to compensate for the scarcity of preferred foods, beyond fissioning and resorting to a generalized diet, macaques will also alter ranging and feeding patterns to adjust to changing climatic and demographic conditions. For Japanese macaques who live in subtropical to subalpine conditions, the pressures of resorting to fall back food in colder seasonal periods creates a variation in home range and time spent feeding. During these colder seasonal periods, macaques that have to resort to low-quality foods such as bark and buds, and spent more time feeding in order to meet energetic requirements to stay warm and avoid hunger (Agetsuma 1995). In order to meet these requirements, and in addition to more time being spent feeding, home range patterns increase to find more food which is scarce (Hanya et al. 2008). More food is necessary to compensate for the lower quality and the energetic requirements spent on acclimating to the seasonal climate. In colder temperate seasons, Japanese macaques change their ranging and feeding patterns to adjust to limited food resources while meeting requirements. Macaques in tropical climates have different ranging behavioral responses to shifts in food availability.
In tropical locations, food availability is not heavily dependent on seasonal changes. Instead, it is dependent upon the quality of habitat. For Tonkean macaques (M. tonkeana), ranging patterns in human altered habitats adjusted in a substantially different manner compared to Japanese macaques in seasonal temperate climates when food is scarce. Instead of modifying food intake and increasing home range, Tonkean macaques shift to occupy other places within their habitat. In a habitat that has been anthropogenically altered by deforestation, Tonkean macaques adjusted by increasing their home range and utilized limited areas with reliable resources in terms of available trees for high-quality food foraging and resting opportunities (Riley 2008). By using both of these strategies, the macaques exploit the higher-quality resources in order to increase survival by relying on smaller numbers of better resources. This strategy suggests Tonkean macaques are plastic as they adjust new strategies of increasing home range and exploiting reliable, available resources in light of changing habitats.
A group of Tonkean macaques (Macaca tonkeana). (Photo by: WikiMedia Commons)
For macaques, available resources are dependent upon the geographic region in which they live. While most macaques live on mainland settings and have potential sympatry (and therefore, compete) with other primates, the Japanese macaque and Formosan rock macaque (M. cyclopis) are found on isolated islands in which they are the sole, extant primates. Island biotas are often more vulnerable because of relatively small populations and limited space for endemic species; yet, Japanese and Formosan rock macaque population trends are listed as stable by the IUCN (2008), whereas the other twenty species of macaques have declining population trends. Both of these primates have been able to adapt to their wide range of habitats on their respective islands without competition from others within the same niche such as other primates. In other species where sympatry is involved, such is the case with the lion-tailed (M. silenus) and bonnet macaques (M. radiata), these species attempt to avoid competition with one another by taking on different strategies within their shared habitat. While the lion-tailed macaque has a generalized diet, they are habitat specialists and only reside near wet evergreen forests; bonnet macaques, however, inhabits a wide variety of places and exploits any habitat in which they find food (Sushma and Singh 2006). Unlike the Japanese and Formosan rock macaques, these macaques have pressure from competing with one another for not only food resources—but also the same habitat. Despite this, because of the higher levels of behavioral plasticity in bonnet macaques, this species faces significantly less extinction pressure than does the lion-tailed macaque (IUCN 2008).
Over time, macaques have faced a wide variety of challenges stemming from the plastic behavioral nature of the genus. However, because of its ability to generalize and exploit resources within the environment for its own benefit, the macaque is surviving many of the pressures of climate and demographic change because of the plastic characteristics. Even though there may be decline of high quality, food available to macaques; they can resort to lower quality, fallback foods, and thus, adjust their behavioral responses accordingly in terms of group size, mating seasonality, and demographic sex ratio. Ranging patterns also shift in an attempt to gain higher quality sources or subsist on the available sources. As a result of these generalizing, plastic tendencies, macaques are one of the most successful primates in terms of dietary, social, and ranging capabilities which make them able to accommodate to their changing habitats.
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