Crab-eating macaque

Macaca comes from the Portuguese word , which was derived from makaku, a word in Ibinda, a language of Central Africa (kaku means monkey in Ibinda). 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. Known fossils indicate that crab-eating macaques inhabited the Sunda Shelf since at least early Pleistocene, ~1mya. It is likely that crab-eating macaques were introduced to Timor and Flores (both on the east side of the Wallace line), by humans around 4,000–5,000 years ago. Crab-eating macaques are the only species on both sides of the Wallace line. The possible stages of crab-eating macaque evolution and dispersal were proposed: • Stage 1: more than , crab-eating dispersed into the Sunda Shelf area. Earliest fossil record of crab-eating macaques was found in Java (this collection included H. erectus and leaf monkey species). They probably reached Java by dry land during a period of glacial advance and low sea levels • Stage 2: around 160 thousand years ago, dispersal and isolation of progenitors of the strongly differentiated deep water fringing island populations occurred. These include M.f. umbrosa, M.f. fusca, M.f., tua [fooden includes M.f. philippinensis but their subspecies status is currently under debate]. It is thought that the progenitors of these subspecies reached deep water habitats during the penultimate glacial maximum when sea levels were lower than present. These populations became isolated during the interglacial period around 120 kya • Stage 3: more than 18 thousand years ago, the differentiation of progenitors of populations of the Indochinese peninsula and northern part of the isthmus of Kra occurred. These subspecies include M.f. aurea and M.f. fascicularis. These two subspecies became differentiated before the last glacial maximum • Stage 4: 18 thousand years ago, the dispersal and isolation of progenitors of weakly differentiated deep water fringing island populations occurred (M. f. fascicularis) • Stage 5: less than 18 thousand years ago, the isolation of the progenitors of shallow water fringing island populations and populations in Penida and Lombok (deep water) occurred. These subspecies include M.f. karimondjawae, M.f. atriceps, M.f. condorensis, M.f. fascicularis • Stage 6: 4.5 thousand years ago, the dispersal and isolation of progenitors of populations in eastern lesser Sunda islands (deep water), occurred (M.f. fascicularis). ==Characteristics==

The crab-eating macaque is sexually dimorphic, with males weighing between and females weighing . The height of an adult male is between and for adult females. Its tail is the length of its head and body combined. Dorsal pelage is generally greyish or brownish with a white underbelly with black and white highlights around the crown and face. The face skin is brownish to pinkish except for the eyelids which are white. Adults are usually bearded on and around the face, except for around the snout and eyes. Older females have the fullest beards, with males' being more whisker like. Subspecies on islands seem to have black coloration of their pelage, and large island and mainland subspecies are lighter. Long-tailed macaque (Macaca fascicularis) male head Angkor.jpg|adult male, Cambodia Long-tailed macaque (Macaca fascicularis) female head Angkor.jpg|adult female, Cambodia Long-tailed macaque (Macaca fascicularis) juvenile.jpg|juvenile, Borneo Macaca fascicularis Ao Nang 5.jpg|juvenile, Thailand == Genetics ==

Along the northern part of its range, the crab-eating macaque hybridizes with the rhesus macaque (M. mulatta). It also has been known to hybridize with the southern pig-tailed macaque (M. nemestrina). Hybrids also occur across subspecies too. ==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 – 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 in Thailand 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. ==Conservation==

The crab-eating macaque is listed on CITES Appendix II. Its IUCN Red List status was uplisted in 2020 and again in 2022 from the Least Concern classification in 2008 as a result of declining population resulting from hunting and troublesome interactions with humans, despite its wide range and ability to adapt to different habitats. These interactions include the skyrocketing demand for crab-eating macaques by the medical industry during the COVID-19 pandemic, and the rapid development of the landscape in Southeast Asia. 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==

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. == See also ==