Cynomolgus

Crab-eating macaque[1]
Conservation status
Scientific classification
Kingdom: Animalia
Phylum: Chordata
Class: Mammalia
Order: Primates
Family: Cercopithecidae
Genus: Macaca
Species: M. fascicularis
Binomial name
Macaca fascicularis
Raffles, 1821
Crab-eating macaque range
Synonyms

Macaca irus F. Cuvier, 1818 Simia aygula Linnaeus, 1758[3][4][5][6]

The crab-eating macaque (Macaca fascicularis), also known as the long-tailed macaque, is a cercopithecine primate native to Southeast Asia. It is referred to as the cynomolgus monkey in laboratories.[2] It has a long history alongside humans;[7] they have been alternately seen as agricultural pests,[8] sacred animals in some temples,[9] and more recently, the subject of medical experiments.[7] The crab-eating macaque lives in matrilineal social groups with a female dominance hierarchy,[10] and male members leave the group when they reach puberty.[11] They are opportunistic omnivores [12] and have been documented using tools to obtain food in Thailand and Myanmar.[13] The crab-eating macaque is a known invasive species and a threat to biodiversity in several locations including Hong Kong and western New Guinea.[2] The significant overlap in macaque and human living space has resulted in greater habitat loss,[7] synanthropic living, and inter- and intra-species conflicts over resources.

Etymology

The scientific name of the crab-eating macaque is Macaca fascicularis. Macaca comes from the Portuguese word macaco, which was picked up from makaku, a Fiot (West African language) word (kaku means 'monkey' in Fiot).[14]

Fascicularis is Latin for 'a small band or stripe'. Sir Thomas Raffles, who gave the animal its scientific name in 1821, did not specify what he meant by the use of this word. In Indonesia and Malaysia, M. fascicularis and other macaque species are known generically as kera, possibly because of the high-pitched cry of the animal.[15]

This animal has several common names. It is often referred to as the long-tailed macaque due, unsurprisingly, to its unusually long tail that is often longer than the body.[16] The species is also commonly known as the crab-eating macaque because it is often seen foraging beaches for crabs. Another common name for M. fascicularis is the cynomolgus monkey, which literally means "dog-milker" monkey; this is the name most commonly used in laboratory settings.

Taxonomy

There are 10 subspecies of Macaca fasciularis:

  • Crab-eating macaque, Macaca fascicularis fascicularis, synonym Macaca irus
  • Burmese long-tailed macaque, M. f. aurea
  • Nicobar long-tailed macaque, M. f. umbrosa
  • Dark-crowned long-tailed macaque, M. f. atriceps
  • Con Song long-tailed macaque, M. f. condorensis
  • Simeulue long-tailed macaque, M. f. fusca
  • Lasia long-tailed macaque, M. f. lasiae
  • Maratua long-tailed macaque, M. f. tua
  • Kemujan long-tailed macaque, M. f. karimondjawae
  • Philippine long-tailed macaque, M. f. philippensis [17]

Physical characteristics

Body length of the adult, which varies among subspecies, is 38–55 cm (15–22 in) with comparably short arms and legs. Males are considerably larger than females, weighing 5-9 kilograms (11-20 lb) compared to the 3–6 kg (7-13 lb) of females.[16] The tail is longer than the body, typically 40–65 cm (16–26 in). The upper parts of their body are dark brown with light golden brown tips. The under parts are light grey with a dark grey/brown tail. Crab-eating macaques have backwards directed crown hairs which sometimes form short crests on mid-line. Their skin is black on their feet and ears while the skin on the muzzle is a light grayish pink color. Eyelids often have prominent white markings and white spots are sometimes seen on ears. Males have a characteristic mustache and cheek whiskers, while females have only cheek whiskers. Crab eating macaques have a cheek pouch which they use to store food while foraging. Females show no perineal swelling.[18] They use this tail for balance as they jump distances up to 5 meters (16.4 feet).[16]

Behavior

Group living

Macaques live in social groups that contain three to twenty females, their offspring, and one or many males. The groups usually have fewer males than females. In social groups of macaques, there is a clear dominance hierarchy among females. These ranks remain stable throughout the female’s lifetime and also can be sustained through generations of matrilines. Females have their highest birth rates at approximately ten years of age and completely stop bearing young by age twenty-four.[10]

The social groups of macaques are female-bonded, meaning that males will disperse at the time of puberty. Thus, group relatedness on average appears to be lower than compared to matrilinearity | matrilines. There is more difference in relatedness when comparing high-ranking lineages to lower ranking lineages, with higher-ranking individuals being more closely related to one another. Additionally, groups of dispersing males born into the same social groups display a range of relatedness, at times appearing to be brothers while at other times appearing to be unrelated.[11]

In addition to the matrilineal dominance hierarchy, there are also male dominance rankings. Alpha-males have a higher frequency of mating compared to their lower-ranking conspecifics. The increased success is due partially to his increased access to females and also due to female preference of an alpha male during periods of maximum fertility. Though females have a preference for alpha males, they do display promiscuous behavior. Through this behavior, females risk helping to rear a non-alpha offspring, yet benefit in two specific ways, both in regard to aggressive behavior. First, there is decreased value placed on one single copulation. Moreover, the risk of infanticide is decreased due to the uncertainty of paternity.[19]

Increasing group size leads to increased competition and energy spent trying to forage for resources, and in particular, food. Further, social tensions build and the prevalence of tension-reducing interactions like social grooming fall with larger groups. Thus, group living appears to be maintained solely due to the safety against predation.[20]

Conflict

Group living in all species is dependent on tolerance of other group members. In long-tailed macaques, successful social group living maintains that there must be post-conflict resolution. Usually, less dominant individuals will lose to a higher-ranking individual when conflict arises. After the conflict has taken place, lower-ranking individuals tend to fear the winner of the conflict to a greater degree. In one study, this was seen by the ability to drink water together. Post-conflict observations showed a staggered time between when the dominant individual begins to drink and the subordinate. Long-term studies reveal that the gap in drinking time closes as the conflict moves further into the past.[21]

Grooming and support in conflict among primates is considered to be an act of reciprocal altruism. In long-tailed macaques, an experiment was performed in which individuals were given the opportunity to groom one another under three conditions: after being groomed by the other, after grooming the other, and without prior grooming. After a grooming took place, the individual who received the grooming was much more likely to support its groomer than one who had not previously groomed that individual. These results support the reciprocal altruism theory of grooming in long-tailed macaques.[22]

Long-tailed macaques demonstrate two of the three forms of suggested post-conflict behavior. In both captive and wild studies, the monkeys demonstrated reconciliation, or an affiliative interaction between former opponents, and redirection, or acting aggressively towards a third individual. Consolation was not seen in any study performed.[23]

Post-conflict anxiety has been reported in long-tailed macaques that have acted as the aggressor. After a conflict within a group, the aggressor appears to scratch himself at a higher rate than before the conflict. Though the scratching behavior cannot definitely be termed as an anxious behavior, evidence suggests that this is the case. An aggressor’s scratching decreases significantly after reconciliation. This suggests that reconciliation itself rather than a property of the conflict is the cause of reduction in scratching behavior. Though these results seem counter-intuitive, the anxiety of the aggressor appears to have a basis in the risks of ruining cooperative relationships with the opponent.[24]

Kin altruism and spite

In a study, a group of long-tailed macaques were given ownership of a food object. Unsurprisingly, adult females favored their own offspring by passively, yet preferentially, allowing them to feed on objects that they held. Interestingly, when juveniles were in possession of an object, mothers robbed them and acted aggressively at an increased rate towards their own offspring compared to other juveniles. These observations suggest that close proximity influences behavior in ownership, as a mother’s kin are closer to her on average. When given a nonfood object and two owners, one being a kin and one a non-kin, the rival will choose the older individual to attack regardless of kinship. Though the hypothesis remains that mother-juvenile relationships may facilitate social learning of ownership, the combined results clearly point to aggression towards the least threatening individual.[25]

A study was conducted in which food was given to 11 females. They were then given a choice to share the food with kin or non-kin. The kin altruism hypothesis suggests that the mothers would preferentially give food to their own offspring. Yet 8 out of the 11 females did not discriminate between kin and non-kin. The remaining 3 did, in fact, give more food to their kin. The results suggest that it was not kin selection, but instead spite that fueled feeding kin preferentially. This is due to the observation that food was given to kin for a significantly longer period of time than needed. The benefit to the mother is decreased due to less food availability for herself and the cost remains great for non-kin due to not receiving food. If these results are correct, long-tailed macaques are unique in the animal kingdom, as they appear not only to behave according to the kin selection theory but also act spiteful toward one another.[26]

Reproduction

After a gestation period of 162–193 days, the female gives birth to one infant. The infant's weight at birth is approximately 320 grams (11 oz).[12] Infants are born with black fur which will begin to turn to a yellow-green, grey-green, or reddish-brown shade (depending on the subspecies) after about three months of age.[16] This natal coat may indicate to others the status of the infant, and other group members treat infants with care and rush to their defense when distressed. Immigrant males will sometimes kill infants not their own, and high-ranking females sometimes kidnap the infants of lower-ranking females. These kidnappings usually result in the death of the infants, as the other female is usually not lactating. Young juveniles stay mainly with their mother and relatives. As male juveniles get older, they become more peripheral to the group. Here they play together, forming crucial bonds that may help them when they leave their natal group. Males that emigrate with a partner are more successful than those that leave alone. Young females, on the other hand, stay with the group and become incorporated into the matriline into which they were born.[27]

Male crab-eating macaques will groom females to increase the chance of mating. A female is more likely to engage in sexual activity with a male that has recently groomed her than with one that has not.[28]

Diet

Crab-eating macaques typically do not consume crabs; rather, they are opportunistic omnivores, eating a variety of animals and plants. Although fruits and seeds make up 60 - 90% of their diet, they also eat leaves, flowers, roots and bark.[12] They sometimes prey on vertebrates (including bird chicks, nesting female birds, lizards, frogs and fish), invertebrates and bird eggs. In Indonesia the species has become a proficient swimmer and diver for crabs and other crustaceans in mangrove swamps. [29]

This species exhibits particularly low tolerance for swallowing seeds. Despite their inability to digest seeds, many primates of similar size will swallow large seeds, up to 25 mm (0.98 in), and simply defecate them whole. The Long Tailed Macaque, on the other hand, spits seeds out if they are larger than 3–4 mm (0.12-0.16 in). This decision to spit seeds is thought to be adaptive; it avoids filling the monkey’s stomach with wasteful bulky seeds that cannot be used for energy.[30]

Although the species is ecologically well-adapted and poses no threat to population stability of prey species in its native range, in areas where the crab-eating macaque is not native, it can pose a substantial threat to biodiversity.[31] Some believe that the crab-eating macaque is responsible for the extinction of forest birds by threatening critical bird breeding areas [32] as well as eating the eggs and chicks of endangered forest birds.[18]

The crab-eating macaque can become a synanthrope, living off human resources. They are known to feed in cultivated fields on young dry rice, cassava leaves, rubber fruit, taro plants, coconuts, mangos and other crops, often causing significant losses to local farmers.[8] In villages, towns, and cities, they frequently take food from garbage cans and refuse piles.[8] The species can become unafraid of humans in these conditions, which can lead to macaques directly taking food from people, both passively and aggressively.

Tool use

In Thailand and Myanmar, long-tailed macaques use stone tools to open nuts, oysters and other bivalves, and various types of sea snails (nerites, muricids, trochids, etc.) along the Andaman sea coast and offshore islands.[13]

Another instance of tool use is the washing and rubbing of foods such as sweet potatoes, cassava roots, and papaya leaves before consumption. Long tailed macaques will either soak these foods in water or rub them through their hands as if to clean them. The monkeys also peel the sweet potatoes, using their incisor and canine teeth. It appears as though adolescents learn these behaviors through the observations of older individuals.[33]

Distribution and habitat

The crab-eating macaque lives in a wide variety of habitats, including primary lowland rainforests, disturbed and secondary rainforests, shrubland, and riverine and coastal forests of nipa palm and mangrove. They also easily adjust to human settlements; they are considered sacred at some Hindu temples and on some small islands,[9] but a pest around farms and villages. Typically, they prefer disturbed habitats and forest periphery. The native range of this species includes most of mainland Southeast Asia, from extreme Southeastern Bangladesh down through Malaysia, and the Maritime Southeast Asia islands of Sumatra, Java, and Borneo, offshore islands, the islands of the Philippines, and the Nicobar Islands in the Bay of Bengal. This monkey is a rare example of a terrestrial mammal that violates the Wallace Line.[18]

Introduced Range

M. fascicularis is an introduced alien species in several locations, including Hong Kong, western New Guinea, Anggaur Island in Palau, and Mauritius. Where it is not a native species, particularly on island ecosystems whose species often evolved in isolation from large predators, M. fascicularis is a documented threat to many native species.[18] This has led the World Conservation Union (IUCN) to list M. fascicularis as one of the "100 worst invasive alien species".[34] Insofar as it is present as an invasive alien species on several islands, it has been labelled a "weed" species and is yet another significant ecological threat to those ecosystems and the species within them. However, M. fascicularis is not a threat to biodiversity in its native range.

The immuno-vaccine Porcine Zona Pellucida (PZP) which causes infertility in females is currently being trialed in Hong Kong to investigate its use as potential population control.[18]

Relationship with humans


Long-tailed macaques extensively overlap with humans across their range in Southeast Asia. Consequently, people and long-tailed macaques live together in many locations. Some of these areas are associated with religious sites and local customs, such as the temples of Bali in Indonesia, Thailand, and Cambodia, while other areas are characterized by conflict as a result of habitat loss and competition over food and space.[7] Humans and long-tailed macaques have shared environments since prehistoric times, and tend to both frequent forest and river edge habitats. Crab-eating macaques are occasionally used as a food source for some indigenous forest dwelling peoples. In Mauritius, they are captured and sold to the pharmaceutical industry, and in Angaur and Palau they are sold as pets.[18] Macaques feed on sugar cane and other crops, affecting agriculture and livelihoods, and can be aggressive towards humans. Macaques may carry potentially fatal human diseases, including B-virus.[18]

In scientific research

M. fascicularis is also used extensively in medical experiments, in particular those connected with neuroscience and disease. Due to their close physiology, they can share infections with humans. Some cases of concern have been an isolated event of Reston ebolavirus found in a captive-bred population shipped to the US from the Philippines, which was later found to be a strain of Ebola that has no known pathological consequences in humans, unlike the African strains.[7] Furthermore, they are a known carrier of monkey B virus (Herpesvirus simiae), a virus which has produced disease in some lab workers working mainly with rhesus macaques (M. mulatta).[7] Nafovanny, the largest facility for the captive breeding of nonhuman primates in the world, houses 30,000 macaques . The crab-eating macaque is one of the types of monkeys that have been used as space test flight animals . It has been discovered recently that Plasmodium knowlesi, which causes malaria in M. fascicularis, can also infect humans. A few cases have been documented in human, but for how long humans have been getting infections of this malarial strain is unknown. It is, therefore, not possible to assess if this is a newly emerging health threat, or if just newly discovered due to improved malarial detection techniques.[7] Given the long history of humans and macaques living together in SE Asia, it is likely the latter.

Conservation status

The crab-eating macaque has the third-largest range of any primate species, behind only humans and rhesus macaques. The IUCN Red List categorizes the species as Least Concern, and CITES lists them as Appendix II ("not necessarily threatened with extinction", in which trade must be controlled to avoid use incompatible with their survival). A recent review of their populations suggests a need for better monitoring of populations due to increased wild trade and rising levels of human-macaque conflict, which are reducing overall population levels despite the species being widely distributed.[35]

Each subspecies faces differing levels of threats, and there is too little information on some subspecies to assess their conditions. The M. f. umbrosa subspecies is likely of important biological significance and has been recommended as a candidate for protection in the Nicobar Islands, where its small, native population has been seriously fragmented,[36] and is listed as vulnerable on the IUCN Red List.[2] The Philippine long-tailed macaque (M.f. philippensis) is listed as near threatened, and M.f. condorensis is vulnerable.[2] All other subspecies are listed as data deficient and need further study;[2] although recent work is showing M.f aurea and M.f. karimondjawae need increased protection.[36] One concern for conservation is, in areas where M. fascicularis is not native, their populations need to be monitored and managed to reduce their impact on native flora and fauna.[36]

See also

References

External links

  • Bonadio, C. 2000. "Macaca fascicularis" (On-line), Animal Diversity Web. Accessed March 10, 2006.
  • Factsheet
  • BBC Factfile on M. fascicularis
  • Vietnam.
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