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Archive for the ‘Macaques’ Category

Yesterday morning, I woke up at 5am to winds at a high speed. About thirty seconds later, there was a torrential downpour. A minute after that, tornado sirens rang. In the course of three minutes after the alarms, my significant other and I had gotten up, put on suitable clothes and shoes, corralled the cats into their carrier, and booked it downstairs to the first floor of our apartment.  Fortunately, not much came of it and both of us came up within fifteen minutes. While nothing happened, my general instinct was to go to the area in which we would be the safest.

This is an instinct we share with multiple animals, but particularly so with our evolutionary ancestors.

A few weeks back, a chemical explosion occurred in a chemical plant near the New Iberia Research Center, a primate research institute which contains 360 chimpanzees and 6,500 new and old world monkeys.  While the wind blew the smoke north, rather than west closer to the primate research center, individuals outside the facility could feel the strong heat.

The researchers also noticed an interesting reaction from the primates as the incident occurred; the rhesus macaques housed outside were quick to drop from their perches for enrichment and get as close to the ground as possible to avoid overheating.   According to the director of the facility, Thomas Rowell, “The animals nearest the incident were down at the bottom of the cages, eating and milling about. The intensity of the heat, if you were standing … was overwhelming. At ground level, there was little, if any heat. They were smart enough to squat on the ground and not expose themselves to the intense heat.”

While there have been no signs of stress or illness, staff will be monitoring the primates to ensure individuals weren’t exposed to chemicals from the plant.

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This post was chosen as an Editor's Selection for ResearchBlogging.org Among the many ecological models of behavior, cognition is one that demonstrates an organism’s mental capacity in response to its environment.  While cognition has been studied widely in humans, in the last two hundred years, cognition with an ethological framework has given greater insights to both behavioral ecology and evolutionary psychology.  Many animals, including elephants, pigs, corvids, and non-human primates have displayed evidence of cognition.  It is believed that over time, cognitive skills were an adaptive response to social living, helping individuals to avoid predators, and to complete other daily activities.  As a further response to this social living, encephalization progressed, allowing individuals to take on complex roles within groups.  Due to these complex roles, greater cognitive specialization occurred because of the greater drive of social relationships within the organism’s environment.  Cognitive specialization ranges from the ability to determine another individual’s thoughts (theory of mind) to making false alarm calls with no predation risk present (deception).  Through these specializations, the individual is better able to respond to changes within the environment in which it lives. Overall, the study of cognition as an ecological model of behavior serves as a method of understanding adaptations in terms of an organism’s sociality driving encephalization, which later allowed for complex information processing relating to behavioral flexibility in maximizing the benefits which result from cognition.

Cognition serves as a method for examining what an individual knows and how it knows what it knows.  The term, cognition, is Latin for “to know, conceptualize, or recognize.”  It is also studied in multiple academic disciplines including psychology, computer science, neuroscience, philosophy, and anthropology.  Within these disciplines, it is examined within an ecological and evolutionary paradigm of understanding the mental constructs of information. Elements of cognition that are frequently studied include attention, memory, perception, judgment, recognition, reasoning, planning, awareness, problem solving, emotion, and communication. Processes in which cognition can occur are contextual; it can be conscious or unconscious and natural or artificial.  Cognition, while encompassing many elements, is also sometimes difficult to define; however, a working definition suggests cognition as a form of information processing and translating of knowledge.

An infant bonnet macaque (Macaca radiata) chewing on a stick to displace its anxiety, perhaps? (Image from: Wild Animal World)

The framework of cognition within the context of an ecological evolutionary concept of information processing is linked to another context: sociality.  Sociality, for many anthropological evolutionary scientists, is believed to be the catalyst for developing a greater cognitive potential in response to an increased overall fitness as sociality increased an individual’s fitness within a group.  Through socially driven responses such as foraging strategies or predator calls, individuals are able to protect and increase their individual fitness by adjusting their reactions according to the specific situation.

Even though most cognition studies are conducted in captivity, there have been some studies performed in the field.  One of the examples of cognitive studies in nature is the examination of deception. Deception is considered a tactical form of cognition in the context of a communication in a social group.  In primates and many other organisms, communication is considered costly for an individual as transmitting a signal requires energy to produce and can reveal the location and status of an individual to predators.  When deception tactics are used, it is thought there is an extra element of expense involved.  Yet, the behavior manages to survive within a behavioral repertoire of some organisms, suggesting there may be some benefit to using tactical deception despite these costs.

In wild bonnet macaques (Macaca radiata), when an aggressor confronts an individual, there are a few options in terms of responses, the individual might choose to flee, to remain and challenge the aggressor, or to remain and ignore the aggressor.  It is thought that if the individual chooses to remain, it may use a technique called “concealment by ignoring.”  Concealment by ignoring is a form of tactical deception wherein an individual chooses to not fight back directly, but displaces any behavior upon a nearby object such as chewing on a twig, while ignoring the nearby aggressor and hiding any expression of fear or stress (Sinha 2003).  In this particular case, the individual is thought to be using deception as instead of fighting or fleeing by hiding its actual response.

According to Whiten and Byrne, for a behavior to be considered as a deceptive tactic, there are two specific requirements: the behavior must be part of the “normal” repertoire and it must be uncommon and varied from contexts in which the behavior would normally appear (1988).  Under these requirements, the example of the bonnet macaques’ concealment by ignoring would be considered as a deceptive tactic.  Bonnet macaques have been known to chew on twigs, but typically only when food is scarce rather than when confronted by a predator (Towner 2010).  Therefore, while this behavior is normal under certain ecological circumstances, it is abnormal in terms of the context in which it occurs; for that reason, the behavior is considered deceptive.

A bonnet macaque showing off a potential "cost" of getting caught for using deceptive tactics. (Image from IronAmmonite.com)

Because deception is meant to be used sparingly, it is difficult to perceive how deception may have evolved as a behavior.  After all, the costs of deception are high as individuals can be targeted for aggression, desensitizing group members to not trust the deceptive individual over time, and the skeptical responses thereof (Gouzoules & Gouzoules 2011).  The skeptical responses are themselves a response to the desensitization of individuals using deceptive alarm calls too frequently; group members that avoid responding to alarm calls may risk predation or other threats.  Still, individual fitness can be increased if deception is used infrequently, as individuals can use deception to their benefit such as monopolizing food resources instead of sharing, Despite the costs, deception persists as a cognitive behavior, suggesting the benefits from the behavior outweigh the potential costs.

One of the suggested explanations for the persistence of deception as a behavior relates back to encephalization.  If sociality is the driver for encephalization, it is possible the infrequent uses of and benefits from deception, used in the right situations, can help an individual’s fitness where net costs are not incurred, enabling individuals to pass on the traits of an enlarged brain to potential future offspring.  Additionally, there is evidence to suggest that the rates and use of deception were correlated with neocortical volume in the primate brain, while there was no association between volume of other parts of the brain or to variations in group sizes within 18 examined primate species (Byrne & Corp 2004).  These findings reflect the idea in which social groups may restrain the cognitive abilities of individuals, as group sizes tend to be an amalgamation of multiple factors including ecological constraints.  Thus, rapid learning leading to deception may result from competition within group members as a strategy for individual fitness.

Even though this idea paints an image of competition being the force in which cognition (and therefore, deception) evolves, this is only a part of it.  After all, group living is sufficient for cognition because adaptations have allowed them to live comfortably within social groups as opposed to solitary living (Barrett & Henzi 2005; Holekamp 2006).  Individuals who negotiate with other group members are thought of as cognitive, as they are thought to process information for their individual fitness benefit as well as the collective group benefit.  Furthermore, negotiation skills are less costly on an individual rather than aggressive tactics as the individual does not have to expend energy fighting back or tending to potential wounds.  Although cognition is studied on an individual level, there is evidence that groups collectively process knowledge as well.

Cognition, from the perspective of a model of evolutionary ecological behaviors, gives individuals an understanding as to how information processing benefits individual fitness in social groups.  While sociality serves as the medium for individuals to adjust their behavior, there are costs and benefits which come from the plasticity of behavioral adjustment.  Costs such as potential aggression for using deceptive tactics.  However, it seems the benefits of receiving access to higher quality such as fruits by having a mental map or occasionally deceiving group members to avoid fights might override the costs.  As an organism processes information within the world around itself and acts flexibly on the received knowledge, the individual is responding to the environmental pressures in which it lives through cognition.

Resources

Barrett, L. & Henzi, P. (2005). The social nature of primate cognition. Proc R Soc Lond B, 272: 1865-1875.

Byrne, R.W. & Corp, N. (2004). Neocortex size predicts deception rate in primates. Proc R Soc Lond B, 271: 1693-1699.

Gouzoules, H. & Gouzoules, S. (2011). The conundrum of communication. In Campbell, C.J., Fuentes, A., MacKinnon, K.C., Bearder, S.K., & Stumpf, R.M. (Eds.), Primates in Perspective, (2nd ed.), (pp. 626-637), New York: Oxford U. Press.

Holekamp, K.E. (2006). Questioning the social intelligence hypothesis. Trends Cog Sci, 30(10): 1-5.

Sinha, A. (2003). A beautiful mind: attribution and intentionality in wild bonnet macaques Current Science, 85 (7), 1021-1031

Towner, S. (2010). Concept of mind in non-human primates. Biosci Horizons, 3(1): 96-104.

Whiten, A., & Byrne, R.W. (1988). Tactical deception in primates. Behav Brain Sci, 11: 233-273.

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Around the world, as the climate begins to change, so too does the primate genus, MacacaMacaca, 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.

 

References

Agetsuma, N.  (1995).  Foraging strategies of Yakushima macaques (Macaca fuscata yakui). Int. J. Primatol. 16: 595-610.

Berman, C.M.  (1988).  Maternal condition and offspring sex ratio in a group of free-ranging rhesus monkeys: an eleven-year study.  Amer. Natural. 131(3): 307-328.

Dittus, W.P.J.  (1998).  Birth sex ratios in toque macaques and other mammals: integrating the effects of maternal condition and competition.  Behav. Ecol. Sociobiol. 44(3): 149-160.

Fooden, J.  (1986).  Taxonomy and evolution of the sinica groups of macaques: 5. Overview of natural history, Field Zool. 29: 1-22.

Fooden, J.  (2000).  Systematic review of the rhesus macaque (Macaca mulatta). Field Zool. 96: 1-179.

Furtbauer, I., Schulke, O., Heistermann, M., & Ostner, J.  (2010).  Reproductive and life history parameters of wild female Macaca assamensisInt. J. Primatol. 31(4): 501-517.

Hai Yin, W. & Richardson, M.  (2008).  Macaca cyclopis. In: IUCN 2010.  IUCN Red List of Threatened Species.  Version 2010.4.  <www.iucnredlist.org>.

Hanya, G., Matsubara, M., Hayaishi, S., Zamma, K., Yoshihiro, S., Kanaoka, M.M., Sugaya, S., Kiyono, M., Nagai, M., Tsuriya, Y., Hayakawa, S., Suzuki, M., Yokota, T., Kondo, D., Takahata, Y.  (2008).  Food conditions, competitive regime, and female social relationships in Japanese macaques: within-population variation on Yakushima. Primates. 49: 116-125.

Menard, N.  (2004).  Do ecological factors explain variation in social organization?  In: Thierry, B., Singh, M., and Kaumanns, W. (eds.), Macaque Societies: A Model for the Study of Social Organization. Cambridge University Press, Cambridge, 237-262.

Mendiratta, U., Kumar, A., Charudutt, M., & Anindya, S.  (2009).  Winter ecology of the Arunachal macaque (Macaca munzala) in Pangchen Valley, western Arunachal Pradesh, northeastern India.  Am. J. Primatol. 71(11): 939-947.

Richard, A.F., Goldstein, S.J., & Dewar, R.E.  (1989).  Weed macaques: the evolutionary implications of macaque feeding ecology.  Int. J. Primatol. 10(6): 569-594.

Riley, E.P., & Prison, N.E.C.  (2010).  Macaques in farms and folklore: exploring the human-nonhuman primate interface in Sulawesi, Indonesia.  Am. J. Primatol. 72: 848-854.

Riley, E.P.  (2007).  Flexibility in the diet and activity patterns of Macaca tonkeana in response to anthropogenic habitat alteration.  Int. J. Primatol. 28(1): 107-133.

Riley, E.P.  (2008).  Ranging patterns and habitat use of Sulawesi Tonkean macaques (Macaca tonkeana) in a human-modified habitat.  Am. J. Primatol. 70(7): 670-679.

Smith, E.O.  (1984).  Non-seasonal breeding patterns in stumptail macaques (Macaca arctoides). Primates. 25(1): 117-122.

Sushma, H.S., & Singh, M.  (2006).  Resource partitioning and interspecific interactions among sympatric rainforest arboreal mammals of the Western Ghats, India.  Behav. Ecol. 17(3): 479-490.

Watanabe, K. & Tokita, K.  (2008).  Macaca cyclopis. In: IUCN 2010.  IUCN Red List of Threatened Species.  Version 2010.4.  <www.iucnredlist.org>.

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In the western mountains of “Ape Hill” in Shou-Shan National Park in Taiwan, a group of Formosan rock macaques scurry around, trying to obtain food from a group of curious visitors.  The crowd stands at a distance from the monkeys, but in their hands, they hold a piece of fruit to lure the primate closer.  This tour is an example of the ecotourism which occurs in many of the countries where primates and other wildlife thrive allowing people to get a close view of nature and learn firsthand about animals and their behaviors outside of a zoo.  However, the effects of ecotourism on wildlife habitats can cause considerable damage to ecosystems and to the wildlife affected by human and agricultural intrusion. Additionally, there are problems for humans that live close to primate habitats: tourists feed primates higher-quality, fattier foods, and as a result, primates tend to invade human settlements seeking out similar foods.  There are growing concerns about the safety of both primates and humans when humans are allowed to be close to the primates and provision them with food.  Even though the ecotourism industry allows people to come closer to wildlife and thereby encourages conservation efforts, because of the lack of enforcement of laws, provisioning from human tourists also creates further socioeconomic and conservation concerns for macaques.

In Shou-Shan Nature Park, Taiwan, the country’s sole endemic extant species of primate, the Formosan macaque (Macaca cyclopis) is the main attraction.  This species of macaque typically lives in elevations which can vary from 100 meters to well over 300 meters; depending on where these macaques are situated in this elevation range, their diet may adjust accordingly from fruits to leaves or to invertebrates (Su and Lee 2001).  Formosan macaques are typically considered as generalists due to their ability to adjust to whatever environment they settle given that they can choose to survive on different types of lower-quality or higher-quality food sources.  Typically, the Formosan macaques were provisioned corn by park staff; corn is regarded as a lower-quality food source as well (Ruesto at al. 2010).  This more abundant but lower-quality food source gives more individuals a chance to feed, as opposed to causing one or two individuals to dominate the food source, and thus, lowers intergroup aggression between the primates.

The provisioned higher-quality food sources that the higher ranking macaques tend to fight over usually comes from a different source other than the park staff.  In some cases, tourists have been known to provision the macaques via illegal food carts outside of the entrances that provide high-quality foods such as fruits and vegetables to tourists to entice the monkeys (Hsu et al. 2009).  While these primates are well fed, these tourists often overlook the potential for anthropogenically influenced shifts in typical behavior due to provisioning from the food carts.  Formosan macaques in larger groups (more than 25 members) tend to become more antagonistic towards other group members when provisioning is involved (Hsu et al. 2009).  This is likely a result of contest competition where members have to compete in order to gain the limited food provided by human visitors.

Formosan Rock Macaques

Formosan Rock Macaques sitting on a sign in Taiwan. (Image from Wikipedia by WikiLaurent)

The change to antagonistic behavior is not limited to group members, however.  There is also evidence in macaques that provisioning can lead to aggressive behavior towards humans supplying the food (Hsu et al. 2009, Ruesto et al. 2010, and McCarthy et al. 2009).  Given the fact that macaques have to compete for food, this suggests that macaques are willing to risk confrontation from a potential threat in order to obtain the high-quality foods that tourists tend to provide.  Additionally, it was discovered by Fuentes (2006) when tourists engaged in using food as bait in order to gain the attention of the monkeys, the occurrence of aggressive behavior (including biting and scratching) increased significantly.  Tourists may further perpetuate a cycle of antagonistic behavior by fighting back; in one case, a group of tourists threw rocks at the monkeys after an incident, injuring one and causing the troop to engage in increasingly threatening behavior until park officials intervened (Ruesto et al.  2010, McCarthy et al. 2009).

While using rocks to fight back is not as common an occurrence as providing food for the macaques, and harmful for the tourists and macaques, both actions are subject to punishment by law.  In 2001, the Kaohsiung City Council in Taiwan passed a law discouraging the practice of illegal provisioning with a US $200 fine in place for feeding or harming macaques or other endangered wildlife (Hsu et al. 2009).  Despite this, tourists who engage in or permit harmful behaviors are rarely punished.  After a given day, staff may find fecal matter from pets that come with their owners, as well as leftovers, plastic items, and other garbage remnants lying around the park (Hsu et al. 2009).  Because these items are not “natural,” some wildlife may ingest them and become ill.  Moreover, the fecal matter from the pets may have a role in shifting nitrogen levels within the soil; thus, making it harder for native plants to grow.  Another problem from not enforcing these rules is rooted in the socioeconomic issues related to the macaques that leave the confines of the park. While monkeys that are provisioned with low-quality diets receive enough food to meet energy requirements, the macaques that eat high-quality foods tend to seek out more to satisfy their hunger as high-quality foods are not as abundant.

In order to find these high-quality food resources, the macaques that have been provisioned enough with fruits and vegetables may leave the park area and subsequently discover and forage for more of these richer foods.  In areas where parks are situated near human agricultural activity, macaques have been known to serve as a pest to local farmers.  Before parks began provisioning monkeys with a low-quality diet, dominant macaques in Bali would invade local rice fields and agricultural gardens (Fuentes et al. 2007).  Because the agriculture was grown so close to the parks, macaques increased their foraging efficiency due to the lack of time spent traveling.  This foraging efficiency, however, comes at a price to the nearby farmers as many suffered significant monetary losses due to the macaques’ preference for high-quality, mature fruits such as bananas and papayas (Linkie et al.  2007).  These fruit which tend to sell for high amounts, and given that when macaques forage, they have a tendency to be destructive which creates damages the crops and increases the perception of macaques as pests.

Because they are often seen as pests, and laws against harming the endangered Formosan macaques are not enforced, the local human population may resort to violent tactics aside from throwing rocks to scare the monkeys off.  In some cases where macaques have raided crops, farmers have taken to capturing methods and then beating the primate, using slingshots, firecrackers, firing air guns, or the most drastic of these retaliatory actions: threatening or killing the monkeys with a shotgun (Knight 1999).  This is problematic because ecotourism draws people in to see endangered species of macaques such as the Formosan macaques, baiting them with higher-quality foods and drive them to the point of seeking out higher-quality foods which may be fatal in some cases and further contribute to endangering the overall species by losing an individual.

Currently, there is no easy solution to the problem of limited park staff being able to control provisioning tactics.  However, there have been methods suggested that could be successful given logistical implementation.  Despite the Taiwanese government’s exclusive reliance on national parks and their staff to protect wildlife and the issues resulting from a lack of staff, a potential solution to this particular issue is to only allow a limited number of tourists in at a given time.  In a survey in one entrance alone, it was measured that over 6,000 people visited the park on the weekends and 3,500 on the weekdays (Hsu et al. 2009).  A reduced number can be decided upon by city officials, park staff, and other members of the local government to make sure it meets the standards to which park officials can safely and consistently manage.  In addition, the smaller numbers would make it easier for the park staff to prevent and detect illegal provisioning, littering of waste products, and conflicts between humans and macaques.

The reduced number of visitors may also reduce the amount of human-macaque conflicts outside of the park as well.  As the macaques will have more space that can be used to escape large groups of people, some monkeys will not feel the need to leave the park boundaries and exit into local farmers’ fields.  Additionally, a correlation was discovered in areas provisioned by tourists between adult aggression in macaques and range restriction due to dense human clusters in the park (Fuentes et al. 2007).  If the number of tourists who provision the macaques decreases, then perhaps the intergroup aggression will also diminish, as there would be a lessened need to compete for food resources among higher-ranking individuals.  Although some macaques may still attempt to find higher-quality food sources in local farms, this prevention of provisioning can also prevent an appetite for high-quality food from developing within the primates.

While the macaques who typically venture outward and forage in agricultural gardens or fields or continue agonistic behaviors are typically adult males, there is another option if reducing the number of tourists fails to condense the occurrences of these behaviors.  This proposed measure involves translocating the aggressive macaques to outlying areas or other areas where there are smaller populations (Hsu et al. 2009).  Thus, the macaques would be prevented from exploring the nearby crops and from agonistic encounters with others within the group and human tourists. Because macaques are generalists and adjust fairly well to new places because of their dietary plasticity, it is likely that many of the translocated macaques will be successful in their new environment.

Ultimately, the potential for implementing these changes comes down to financial ability.  The success of these endeavors depends on whether or not the local government is able to pay for the costs of park staff: even if the number of tourists becomes reduced, the laws and park rules may remain unenforced due to an overall shortage of staff to cover the amount of land the park covers.  Moreover, potentially diverting funds from other pressing issues within the government’s budget towards the general staff maintenance of the park may cause even further strife in local communities (Johnson 2009).  Local communities may become resentful towards the government for not allocating more money to their needs and not vote for incumbents or, potentially, not visit the local parks out of protest.  As a result, the local parks lose income, which in turn decreases park-based provisioning of food and protection for macaques.

Across many sites around the world with macaques and other wildlife species, the issue of provisioning takes on a cyclical nature which is not so easy to prevent or solve.  Socioeconomic, wildlife interests, and other elements must be considered before making a decision to rule out potential problems related to the welfare of the macaques and humans, and often remedying one issue increases another.  The responsibility of undertaking regulating wildlife parks for macaques, tourists, and staff is certainly a large one, but when done properly, can enrich, educate, and encourage local community members to protect their wildlife—as is the purpose of ecotourism.

References

Fuentes, A.  (2006).  Human culture and monkey behavior: assessing the contexts of potential
pathogen transmission between macaques and humans.  Am. J Primatol. 68: 880-896.

Fuentes, A., Shaw, E., and Cortes, J.  (2007).  Qualitative assessment of macaque tourist sites
in Padangtegal, Bali, Indonesia, and the Upper Rock Nature Reserve, Gibraltar.
Int. J Primatol. 28: 1143-1158.

Hsu, M.J., Kao, C.C., and Agoramoorthy, G.  (2009).  Interactions between visitors and
Formosan macaques (Macaca cyclopis) at Shou-Shan Nature Park, Taiwan.
Am. J Primatol. 71: 214-222.

Johnson, A.E.  (2009).  Money matters: financial flows and priority setting around Podocarpus
National Park, Ecuador.  J Sustainable Forestry 28: 712-734.

Knight, J.  (1999).  Monkeys on the move: the natural symbolism of  people-macaque conflict in
Japan.  Journal of Asian Studies 58(3): 622-647.

Linkie, M., Dinata, Y., Nofrianto, A., and Leader-Williams, N.  (2007).  Patterns and perceptions
of wildlife crop raiding in and around Kerinci Seblat National Park, Sumatra.
Animal Conservation 10: 127-135.

McCarthy, M.S., Matheson, M.D., Lester, J.D., Sheeran, L.K., Li, J.H., and Wagner, R.S.
(2009).  Sequences of Tibetan macaque (Macaca thibetana) and tourist behaviors at
Mt. Huangshan, China.  Primate Conservation 24: 145-151.

Ruesto, L.A., Sheeran, L.K., Matheson, M.D., Li, J.H., Wagner, R.S.  (2010).  Tourist behavior
and decibel levels correlate with threat frequency in Tibetan macaques (Macaca
thibetana) at Mt. Huangshan, China.  Primate Conservation 25: 1-6.

Su, H.H., and Lee L.L.  (2001).  Food habits of Formosan Rock Macaques (Macaca cyclopis)
in Jentse, Northeastern Taiwan, assessed by fecal analysis and behavioral observation.
Int. J Primatol. 22(3): 359-378.

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Admittedly, I’ve been a little too pre-occupied with other things than blogging right now. I found out a few weeks ago I’d be losing my position at the primate library I work at because we lost a major grant that sustained our department, so I’ve been busy with trying to find a job and getting ready to move into a new apartment. That said, I don’t have anything extremely insightful for anyone and probably won’t until classes get started up again in September. Until then, enjoy!

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Although I’ve already wrote about this subject before, I think it deserves a little more attention. It’s also a little belated, but yesterday marked the 50th year of Jane Goodall’s study at the Gombe site.  I believe I would be extremely hard-pressed to find any primatologist that hasn’t been touched in some way by Goodall and her studies, and even non-primatologists have heard of and know of Goodall’s research. As someone who wants to go into primatology, I can’t not think about it without Goodall’s contributions.

Goodall recreated what it meant to be human when she discovered that chimpanzees use tools for nut-cracking or for termite “fishing.” She found that war may not necessarily be a human-only event in the 1970’s when war broke out between Kasakela males and other males of splinter groups. She also discovered hunting and meat-eating in these primates when after following a chimpanzee named “David Greybeard” was eating part of a baby bushpig. Moreover, she also debunked a solid then-fact as to what it meant to be human: bipedal, as the chimpanzees were often bipedal. Without this information, anthropology and many other fields could not have advanced to where it is today as to define what a “human” really is–a giant, upright ape among many other things.

Over the past 50 years, Goodall has also contributed to the world of wildlife conservation as well by empowering local individuals and bringing the chimpanzee’s stories to light. Additionally, through her Jane Goodall Institute and programs such as Roots and Shoots, she is able to tour schools and give talks to children to inspire them to become environmentalists and give and work for conservation efforts.

But I think the most important thing Goodall has taught people, be it in research or in conservation and everything else in life–is not to give up in the face of adversity. To me, Jane Goodall is a symbol for what I should aspire to attain–not because of her fame, but what I can contribute myself to the world.

As such, I’ve recently begun thinking about what I want to do for at least some of my life–I love studying and working with primates more than anything I’ve considered before. However, I’m not entirely sure research is for me: I recently quit my job in a lab at the Wisconsin National Primate Research Center and I realize that I don’t really miss it at all. I’m not talented at math in the least either, and honestly, captive studies in research centers bore me (although, admitedly–I have not attempted captive free-range research as the WNPRC does not allow for this being in cold Wisconsin and all.) I liked being out in Costa Rica and watching the primates interact with their wild settings, but I’m still not sure research is my niche.

Instead, I want to work more with conservation. More specifically than this, conservation laws. I want to be able to help curb bushmeat trade in Europe and other places, I want to make reasonable laws that prevent overhunting of primates everywhere, and I want to be able to prevent overlogging areas in which primates thrive.  I want to make sure that when primate research is done in the U.S. and elsewhere that it’s performed as ethically and humanely as possible and that it also contributes to the primate’s well-being as well. Here, I guess I am proposing a new field of primatology–legal primatology. If there’s medical primatology and ethnoprimatology, why can’t there be legal primatology?

I hope to make this a reality; I’ll be applying to law schools instead this coming year and I could not have even considered this potential line of work without Jane Goodall–and numerous other primatologists’ thankless work as well. I’m grateful for everything Jane has done, will do, and those who choose to follow in her and many others’ paths as well. To that, I say thank you and here’s to hopefully another 50 years and more at Gombe.

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I recently finished off my Primate Conservation course and it really opened my eyes a lot. I’m really, really grateful for having the ability to have taken that class and for the professor for teaching that class. She’s a fantastic primatologist and someone I really admire for all she’s accomplished. As a result, I find it fitting to write about captive breeding today because I think it’s a subject worth considering as a conservation method for population management, at the very least.

It’s not uncommon for a lot of captive breeding programs to fail miserably when it comes to primates; they’re very expensive to maintain (especially as you go towards the greater apes), they’re social animals, and because we can’t understand some of the communication methods primates use, we can’t fully tend to their needs. Moreover, captive breeding programs that exist to eventually release subjects into the wild also have to be careful about domestication, genetic inbreeding, potential disease transmission, and even the politics of the country of habitat they intend to release individuals back into as to avoid possible slaughter for hungry troops if there’s a war going on. And most importantly: captive breeding staff must be careful to not entirely domesticate and desensitize the individuals from not being able to recognize predators (which includes humans).

Another consideration is the captive environment itself and how it contributes to the potential setback of captive breeding programs.  In strictly captive settings where the primates are kept in a caged or enclosed environment, the potential for disease transmission increases as there are less places to avoid the ill individual. In a study performed by Willete et al. (2007) in a captive setting, rhesus macaques who were injected with lipopolysaccharides were discovered to have a strong leukocyte response (which isn’t surprising, since they act as endotoxins and call for a strong immune response). Also, in this study (and here’s where it’s pertinent to captive breeding programs), they measured the cortisol levels of the macaques at certain points; the one that raised the highest cortisol was when they used the human-intruder paradigm.

Why is that significant? Because the human-intruder paradigm may mirror zoo-goers in a given day. Particularly when its crowds of people and they all may not be gearing their attention towards the primates in question. So if there’s even more people rather than just the one, maybe it’s possible that the increased cortisol can limit reproductive abilities. But that’s just a postulate and may not be applicable to all primates; some may even like the crowds because it gives them something to look at–I’ve seen this with chimpanzees watching the crowds at the Henry Vilas Zoo here.

So my jury is still out on zoos as an effective captive breeding program (sure, it works with golden lion tamarins, but I’m not sure how well it might work out with those primates with slower life histories who are more specialized; if there are any other success stories, I’d love to hear them though!). But, I do think there’s something with semi-captive breeding programs, specifically when they’re in the country of origin.

Specifically, I am thinking of the Peignot et al. (2008) study on the first successful translocation of mandrills in Gabon.  In a released group of 36 captive-bred mandrills who were raised in a semi-captive environment, the mortality rate of the first year was 33% with infants being the most affected individuals.  However, in the second year, the number decreased to 4%.  From what I understood, Peignot et al. attributes this to the mandrills becoming more acclimated to their new environment and becoming accustomed to food availability during seasonal shifts; additionally, the provisioning was eventually reduced and taken away.

So why the success? I think it a lot of it contributes to the fact that mandrills are extremely plastic: they’re opportunistic omnivores and will generally eat anything. However, I’m willing to bet that the consideration to where and how these individuals were raised also plays a part. For instance, these mandrills were raised in semi-captive conditions as opposed to cages or enclosures which allowed for more foraging, more exploration of the environment, and they were able to acclimate to both the temperature and environment since they were raised in the CIMRF (Centre International de Recherches Médicales de Franceville) in Gabon, where they were translocated as well. And because they didn’t have to go through the stressor of being placed on a plane and being shipped to a different country or anything else that may contribute such as that, the program saved themselves a pretty penny and were able to reroute the funds elsewhere.

So, I’m still not sold on the fact that captive breeding is a waste of time and resources. I think there’s legitimacy to the idea that captive breeding can contribute to enhancing populations; I just think there needs to be more considerations given pre-translocation/release to ensure that the released population can be viable.

 

 

References

Peignot, P., Charpentier, M.J.E., Bout, N., Bourry, O., Massima, U., Dosimont, O., Terramorsi, R., & Wickings, E.J.  (2008).  Learning from the first release project of captive-bred mandrills (Mandrillus sphinx) in GabonOryx, 42(1), 122-131.

Willete, A.A., Lubach, G.R., & Coe, C.L.  (2007).  Environmental context differentially affects behavioral, leukocyte, cortisol, and interleukin-6 responses to low doses of endotoxin in the rhesus monkeyBrain, Behavior, and Immunity, 21(6), 807-815.

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