|This article's lead section may not adequately summarize key points of its contents. (December 2012)|
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.
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). 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, although it is presumed it had something to do with his observation of the animal's color.[not in citation given][page needed]
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. 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. In Indonesia, M. fascicularis and other macaque species are known generically as kera, possibly because of the high-pitched alarm calls they give when in danger ("krra! krra!").
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
Body length of the adult, which varies among subspecies, is 38–55 cm (15–22 in) with comparably short arms and legs. The tail is longer than the body, typically 40–65 cm (16–26 in). Males are considerably larger than females, weighing 5-9 kilograms (11-20 lb) compared to the 3–6 kg (7-13 lb) of females.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
After a gestation period of 167–193 days, the female gives birth to one infant. The infant's weight at birth is approximately 350 grams (12 oz). 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. 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.
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.
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. They sometimes prey on vertebrates (including bird chicks, nesting female birds, lizards, frogs and fish), invertebrates and bird eggs. 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.
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. In villages, towns, and cities, they frequently take food from garbage cans and refuse piles. The species can become unafraid of humans in these conditions, which can lead to macaques directly taking food from people, both passively and aggressively.
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.
Distribution and habitat
The crab-eating macaque lives in a wide variety of habitats, including primary lowland rainforests, disturbed and secondary rainforests, 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, 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.
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. This has led the World Conservation Union (IUCN) to list M. fascicularis as one of the "100 worst invasive alien species". 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.
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. Humans and long-tailed macaques have shared environments since prehistoric times, and tend to both frequent forest and river edge habitats.
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. 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). 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. Given the long history of humans and macaques living together in SE Asia, it is likely the latter.
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.
Each subspecies faces differing levels of threats, and there is too little information on some subspecies to asses 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, and is listed as vulnerable on the IUCN Red List. The Philippine long-tailed macaque (M.f. philippensis) is listed as near threatened, and M.f. condorensis is vulnerable. All other subspecies are listed as data deficient and need further study; although recent work is showing M.f aurea and M.f. karimondjawae need increased protection. 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.
- Groves, C. P. (2005). In Wilson, D. E.; Reeder, D. M. Mammal Species of the World (3rd ed.). Baltimore: Johns Hopkins University Press. pp. 161–162. OCLC 62265494. ISBN 0-801-88221-4.
- Ong, P. & Richardson, M. (2008). Macaca fuscicularis. In: IUCN 2008. IUCN Red List of Threatened Species. Retrieved 4 January 2009.
- "Simia fascicularis Raffles, 1821 (Mammalia, Primates): request for the suppression under the plenary powers of Simia aygula Linnaeus, 1758, a senior synonym. Z.N.(S.) 2399". Bulletin of Zoological Nomenclature 40 (2): 117–118. July 1983. ISSN 0007-5167. Retrieved 19 November 2012. "Simia aygula is quite clearly the Crab-eating or Long-tailed Macaque, as Buffon opined as early as 1766."
- J. D. D. Smith (2001). "Supplement 1986-2000". Official List and Indexes of Names and Works in Zoology. International Trust for Zoological Nomenclature. p. 8. Retrieved 19 November 2012. "Suppressed under the plenary power for the purposes of the Principle of Priority, but not for those of the Principle of Homonymy"
- Wilson, D. E.; Reeder, D. M., eds. (2005). "Macaca fascicularis fascicularis". Mammal Species of the World (3rd ed.). Johns Hopkins University Press. ISBN 978-0-8018-8221-0. OCLC 62265494.
- Linnaeus, Carl (1758). Systema naturæ. Regnum animale. (10 ed.). p. 27. Retrieved 19 November 2012.
- Raffles, Sir TS (1821). "Descriptive Catalugue of a Zoological Collection, made on account of the Honourable East India Company, in the Island of Sumatra and its Vicinity....". Transactions of the Linnean Society.
- van Noordwijk, Maria, and Carcel van Schaik (January 1999). "The Effects of Dominance Rank and Group Size on Female Lifetime Reproductive Success in Wild Long-tailed Macaques, Macaca fascicularis". Primates 40: 105–130.
- de Ruiter, Jan, and Eli Geffen (October 1998). "Relatedness of matrilines, dispersing males and social groups in long-tailed macaques (Macaca fascicularis)". Proceedings of the Royal Society Biological Sciences 285: 79–87.
- de Ruiter, Jan, Jan van Hooff, and Wolfgang Scheffrahn (June 1995). "Social and Genetic Aspects of Paternity in Wild Long-Tailed Macaques (Macaca fascicularis)". Behaviour 129: 203–224.
- Schaik, Carel, Maria Noordwijk, Rob Boer, and Isolde Tonkelaar (April 1983). "The effect of group size on time budgets and social behavior in wild long-tailed macaques". Behavioral Ecology and Sociobiology 13: 173–181.
- Cords, Marina (December 1992). "Post-conflict reunions and reconciliation in long-tailed macaques". Animal Behavior 44: 57–61.
- Hemelrijk, Charlotte (February 1994). "Support for being groomed in long-tailed macaques, Macaca fascicularis". Animal Behavior 48: 479–481.
- Aureli, Filippo (June 1992). "Post-conflict behaviour among wild long-tailed macaques, (Macaca fascicularis)". Behavioral Ecology and Sociobiology 31: 329–337.
- Das, Marjolijn, Zsuzsa Penke, and Jan van Hoof (1998). "Potconflict Affiliation and Stress-Related Behavior of Long-Tailed Macaque Aggressors". International Journal of Primatology 19: 53–71.
- Kummer, Hans and Marina Cords (December 1991). "Cues of ownership in long-tailed macaques, Macaca fascicularis". Animal Behavior 42: 529–549.
- Schaub, Hanspeter (1996). "Testing Kin Altruism in Long-Tailed Macaques (Macaca fascicularis) in a Food-sharing Experiment". International Journal of Primatology 17: 445–467.
- Gumert, Michael D. (December 2007). "Payment for sex in a macaque mating market". Animal Behavior 74 (6): 1655–1667. doi:10.1016/j.anbehav.2007.03.009.
- Gumert, MD; Kluck, M., Malaivijitnond, S. (2009). "The physical characteristics and usage patterns of stone axe and pounding hammers used by long-tailed macaques in the Andaman Sea region of Thailand". American Journal of Primatology 71: 594–608.
- "100 of the world's worst invasive alien species" (PDF). Invasive Species Specialist Group/IUCN. Archived from the original on 2007-07-15. Retrieved 2007-10-21.
- Gumert, MD, Fuentes A, Jones-Engel, L. (2011). Monkeys on the Edge: Ecology and Management of Long-tailed Macaques and their Interface with Humans. Cambridge University Press.
- Eudey, Ardith (2008). "The crab-eating macaque (Macaca fascicularis) widespread and rapidly declining.". Primate conservation 23: 129–132.
- Umapathy, G.; Singh M., Mohnot, S.M. (2003). "Status and Distribution of Macaca fascicularis umbrosa in the Nicobar Islands, India". International Journal of Primatology 24: 281–293.