Crab-eating macaque

The crab-eating macaque (Macaca fascicularis), also known as the long-tailed macaque or cynomolgus macaque, is a macaque species native to Southeast Asia. As a synanthropic species, the crab-eating macaque thrives near human settlements and in secondary forests. The crab-eating macaque has developed a variety of cultural perceptions, from being smart and adaptive, to being sacred, to even being pests in some cases.

The crab-eating macaque is omnivorous and frugivorous. It lives in matrilineal groups ranging from 10 to 85 individuals, with groups exhibiting female philopatry and males emigrating from natal group at puberty. The crab-eating macaque is the only old-world monkey known to use stone tools in their daily foraging, and it engages in a robbing and bartering behavior in some tourist locations.

The crab-eating macaque is the most traded primate species and also the most popular species used in scientific research. Due to these threats, the crab-eating macaque was listed as Endangered on the IUCN Red List in 2022. The specific epithet 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, the crab-eating macaque and other macaque species are known generically as kera. Another common name for M. fascicularis, often used in laboratory settings, is the cynomolgus monkey which derives from Greek Kynamolgoi meaning "dog milkers". It has also been suggested that cynomolgus refers to a race of humans with long hair and handsome beards who used dogs for hunting according to Aristophanes of Byzantium, who seemingly derived the etymology of the word cynomolgus from the Greek κύων, cyon 'dog' (gen. cyno-s) and the verb , 'to milk' (adj. amolg-os), by claiming that they milked female dogs.

Perceptions and terminology

The crab-eating macaque is understood and perceived in many ways: smart, pestiferous, exploited, sacred, vermin, invasive.

In 2000 the crab-eating macaque was placed on the list of 100 most invasive species. For example, it is considered an invasive alien species (IAS) on Mauritius, articles argue for long-tailed macaques spreading seeds of invasive plants, competing with native species like the Mauritian flying fox, and having a detrimental impact on native threatened species. Several authors pointed out that the present evidence indicates that predation on birds by monkeys may have been overestimated. Some address these accusations and they point out the crab-eating macaques do not prefer primary forest thus it is unlikely that Mauritius macaques were ever a major source of indigenous forest destruction. The primary driver of bird extinction has been habitat destruction by humans. Sussman and Tattersall mention that the Dutch abandoned the island in 1710–1712 due to monkeys and rats destroying plantations, they point out that the human population was low at this time and the crab-eating macaques would have had plenty of primary forest to exploit, yet they chose to brave the dangers of raiding plantations. They do not deny that macaques on Mauritius prey on bird eggs and disseminate seeds of exotic plants yet the major loss of species on Mauritius is due to habitat loss caused by humans – macaques are successful because they prefer secondary forest and disturbed habitats.

Taxonomy

Ten subspecies of the crab-eating macaque were proposed:

Evolution

The macaque originated in northeastern Africa some 7 million years ago and spread through most of continental Asia by , and subdivided into four groups (sylvanus, sinica, silenus, and fascicularis). The earliest split in the genus Macaca likely occurred ~4.5 mya between an ancestor of the silenus group and a fascicularis-like ancestor from which non-silenus species later evolved. The species of the fascicularis group (which include m. fascicularis, m. mulatta, and m. fuscata) share a common ancestor that lived 2.5 mya. It is suggested that M. fascicularis are the most plesiomorphic (ancestral) taxon in the fascicularis clade, thus it is argued that M. mulatta evolved from a fascicularis-like ancestor that reached mainland from its homeland in Indonesia around 1 mya.

A phylogenetic analysis found evidence that the fascicularis group originated from an ancient hybridization between the sinica and silenus groups ~3.45–3.56 mya, soon after the initial separation of two parent lineages (proto-sinica and proto-silenus) ~3.86 mya. This divergence and subsequent hybridization occurred during rapid glacial-eustatic fluctuations in the early Pleistocene: high sea levels may have led to the initial separation of proto-sinica and proto-silenus while the subsequent lowering of sea levels facilitated the secondary contact needed for hybridization.

Distribution and habitat

The crab-eating macaque's native range encompasses most of mainland Southeast Asia, through the Malay Peninsula and Singapore, 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 primate is a rare example of a terrestrial mammal that violates the Wallace line, being found out across the Lesser Sunda Islands. It 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. It also easily adjusts to human settlements and is considered sacred at some Hindu temples and on some small islands, but as a pest around farms and villages. Typically, it prefers disturbed habitats and forest periphery.

Introduction to other regions

Humans have transported crab-eating macaques to at least five islands: Mauritius, West Papua, Ngeaur, Tinjil Island near Java, and Kabaena Island off of Sulawesi, and to Kowloon Hills of Hong Kong. From the mid-1980s to mid-1990s the population of crab-eating macaques on Mauritius was estimated at 35,000 to 40,000. The present population is not known but estimates indicate it may be as low as 8,000. On Mauritius macaques are also perceived as sacred, source of tourism, pets, pest, and food. There is little known of the population on Kabaena Island, Sulawesi. These crab-eating macaques appear to have distinct morphology, which may suggest that they have been on the island for a long period of time. This may be a sustainable way of supplying monkeys for research, but it is in a legal gray area for trading regulations, using captive bred codes (F, C) rather than wild-caught (W).

Population size

Because crab-eating macaques are synanthropic, enhancing their visibility to humans, this leads to an overestimation in their population size. Many authors cite a 40% decline in the entire crab-eating macaque population between 1980 and 2006. population estimate of 3 million in 2006. It is unclear how the 3 million estimate was reached.

Using a noninvasive probability model to estimate the maximum population abundance, it was estimated that the current population of crab-eating macaques is 1 million, which reflects a continuous decline in the population – 80% reduction over 35 years. This study used a model that overestimated population so the true decline is probably even greater. A population Viability Analysis (PVA) for crab-eating macaques revealed that the presence and absence of females in a population are key to its short and long term viability. Anything that negatively targets females is likely to threaten population viability, e.g., harvesting for biomedical research targets females.

Behavior and ecology

The crab-eating macaque is highly adaptive, living near and benefiting from humans and environmental modifications.

Group size and structure

Crab-eating macaques live in matrilineal groups ranging from 10 to 85 members, but most often fall in the range of 35–50. Group size varies greatly, especially between non-provisioned and provisioned groups. Males leave natal group as late juveniles or subadults before the age of seven.

Conflict

Group living in all species is dependent on the tolerance of other group members. In crab-eating macaques, successful social group living requires postconflict resolution. Usually, less dominant individuals 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 in the ability to drink water together. Postconflict observations showed a staggered time between when the dominant individual begins to drink and the subordinate. Long-term studies reveal 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 crab-eating 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 grooming took place, the individual that received the grooming was much more likely to support their groomer than one that had not previously groomed that individual.

Crab-eating macaques demonstrate two of the three forms of suggested postconflict behavior. In both captive and wild studies, they 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. When crab-eating macaques are approached by others while foraging, they tend to move away.

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

Kin altruism and spite

thumb|220px|right|Macaca fascicularis fascicularis at the [[Bukit Timah Nature Reserve – Singapore. Video Clip]]

In a study, a group of crab-eating macaques was given ownership of a food object. Adult females favored their own offspring by passively, yet preferentially, allowing them to feed on the objects they held. 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 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 not, 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 nonkin. The kin altruism hypothesis suggests the mothers would preferentially give food to their own offspring. Yet eight of the 11 females did not discriminate between kin and nonkin. The remaining three did, in fact, give more food to their kin. The results suggest 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 nonkin due to not receiving food. If these results are correct, crab-eating macaques are unique in the animal kingdom, as they appear not only to behave according to the kin selection theory, but also act spitefully toward one another.

Reproduction

After a gestation period of 162–193 days, the female gives birth to one infant. The infant's weight at birth is about . Infants are born with black fur which will begin to turn to a grey or reddish-brown shade (depending on the subspecies) after about three months of age.

Male crab-eating macaques 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.

Studies have found that the dominant male copulates more than other males in the group. DNA tests indicate that dominant males sire most of the offspring in natural crab-eating macaque troops. They exhibit particularly low tolerance for swallowing seeds, and spit seeds out if larger than . 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. Fruit makes up 40% to over 80% of the diet of wild crab-eating macaques, except in highly provisioned populations or highly disturbed environments. In Padangtegal Bali macaque 70% of their diet is provisioned. They become unafraid of humans in these conditions, which can lead to macaques directly taking food from people, both passively and aggressively.

Tool use

thumb|Stone tool usage by crab-eating macaques in [[Laem Son National Park in Thailand]]

thumb|A crab-eating macaque using a stone as tool

The crab-eating macaque is the only old world monkey known to use stone tools in its daily foraging. This has been mainly observed in coastal areas of Thailand and Myanmar. In Thailand, crab-eating macaques use ax-shaped stones to crack rock oysters, detached gastropods, bivalves and swimming crabs; in abandoned plantations, they crack oil palm nuts, which shows their ability to take advantage of anthropogenic changes. Human activities can negatively impact tool-using macaques, thus disrupting the persistence of these stone tool use traditions.

Another instance of tool use is washing and rubbing foods, such as sweet potatoes, cassava roots, and papaya leaves, before consumption. Crab-eating macaques either soak these foods in water or rub them through their hands as if to clean them. They also peel the sweet potatoes, using their incisors and canine teeth. Adolescents appear to acquire these behaviors by observational learning of older individuals.

Robbing and bartering

Robbing and bartering is a behavioral pattern in which free ranging nonhuman primates spontaneously steal an object from a human and then hold onto that object until that or another human solicits an exchange by offering food. This behavior is seen in crab-eating macaques at Uluwatu population in Bali, and is described as a population specific behavioral practice, prevalent and persistent across generations and characterized by marked intergroup variation. Synchronized expression of robbing and bartering was socially influenced and more specifically explained by response facilitation. This result further supports the cultural nature of robbing and bartering. Token-robbing and token/reward-bartering are cognitively challenging tasks for the Uluwatu macaques that revealed unprecedented economic decision-making processes, i.e., value based token selection and payoff maximization. This spontaneous, population specific, prevalent, cross-generational, learned and socially influenced practice may be the first example of a culturally maintained token economy in free-ranging animals.

Threats

The crab-eating macaque has been categorized as Endangered on the IUCN Red List; it is threatened by habitat loss due to rapid land use changes in the landscapes of Southeast Asia and the surging demand by the medical industry during the COVID-19 pandemic.

Each subspecies faces differing levels of threats, and too little information is available on some subspecies to assess their conditions. M. f. umbrosa 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. It 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; Crab-eating macaques are sold for up to $20,000 to $24,000, and prices rise when supply reduces. International crab-eating macaque trade does not appear to follow a particular trend but continues to change over time. Although peak exports often correlate with declarations of public health emergences.

In the 1970s, India was the largest supplier of macaques, mostly rhesus macaques, but put a ban on export because when it became apparent that monkeys were used to test military weapons. After this ban, crab-eating macaques began to be used more in biomedical research. Imports of crab-eating macaques in the US and elsewhere began to increase during the worldwide reduction and subsequent ban of rhesus macaque exports from India.

In the 1990s, four major commercial monkey farms operated by Chinese entrepreneurs began exporting wild caught macaques as captive bred, and monkeys smuggled from Laos and Cambodia were likely part of these transactions. Macaques are regularly sold and kept as pets in China, Vietnam, and Indonesia. In Indonesia pet macaques are usually taken from the wild, which was illegal since 2009, but in 2021 the Indonesian government lifted the harvest ban and reinstated a harvest quota. In Indonesia, crab-eating macaques and pig tailed macaques are the only primates that are not included in the list of protected species. Charles River Laboratories is also under investigation. This laundering is a sophisticated trans-border wildlife trafficking network. Crab-eating macaques are harvested in places like Cambodia, Laos, and Myanmar and then laundered through Vietnam and illegally smuggled to places like China.

The Long-Tailed Macaque Project and The Macaque Coalition are engaged in conservation of the crab-eating macaque through research and public engagement.

Relationship with humans

thumb|A crab-eating macaque living in a human vicinity, with a stolen [[asthma inhaler]]

Crab-eating macaques extensively overlap with humans across their range in Southeast Asia. Consequently, they live together in many locations. Some of these areas are associated with religious sites and local customs, such as the monkey forests and 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 crab-eating macaques have shared environments since prehistoric times, and both tend to 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 island in Palau, they are sold as pets.

In places like Thailand and Singapore human-macaque conflict task forces have been created to try and resolve some of these conflicts. they are also used in infectious disease, TB, HIV/AIDS, and neuroscience studies.

The use of crab-eating macaques and other nonhuman primates in experimentation is controversial with critics charging that the experiments are cruel, unnecessary and lead to dubious findings. One of the most well known examples of experiments on crab-eating macaques is the 1981 Silver Spring monkeys case.

In 2014, 21,768 crab-eating macaques were imported in the United States to be used in experimentation.

Clones

On 24 January 2018, scientists in China reported in the journal Cell the creation of two crab-eating macaque clones, named Zhong Zhong and Hua Hua, using the complex DNA transfer method that produced Dolly the sheep.

Abuse scandal

In June 2023, BBC exposed a global online network of sadists who shared videos of baby long-tailed macaques being tortured by caretakers in Indonesia. There were many torture methods, from teasing the primates with baby bottles to killing them in blenders, sawing them in half, or cutting off their tails and limbs. Enthusiasts would pay for the caretakers to film videos torturing the macaques. Investigation has led to some prisons and police searches in both Indonesia and the United States, where many of the torture enthusiasts were located.

References

External links

Bonadio, C. 2000. "Macaca fascicularis" (On-line), Animal Diversity Web. Accessed March 10, 2006.
Primate Info Net Macaca fascicularis Factsheet
ISSG Database: Ecology of Macaca fascicularis
"Conditions at Nafovanny", video produced by the British Union for the Abolition of Vivisection following an undercover investigation at a captive-breeding facility for long-tailed macaques in Vietnam.