El macaco cangrejero (Macaca fascicularis)
The crab-eating macaque (Macaca fascicularis), also known as the long-tailed macaque and referred to as the cynomolgus monkey in laboratories, is a cercopithecine primate native to Southeast Asia. A species of macaque, the crab-eating macaque has a long history alongside humans. The species has been alternately seen as an agricultural pest, a sacred animal, and, more recently, the subject of medical experiments.
The crab-eating macaque lives in matrilineal social groups of up to eight individuals dominated by females. Male members leave the group when they reach puberty. It is an opportunistic omnivore and has been documented using tools to obtain food in Thailand and Myanmar. The crab-eating macaque is a known invasive species and a threat to biodiversity in several locations, including Hong Kong and western New Guinea. The significant overlap in macaque and human living space has resulted in greater habitat loss, synanthropic living, and inter- and intraspecies conflicts over resources.
Etymology
Macaca comes from the Portuguese word macaco, 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, possibly because of their high-pitched cries.
The crab-eating macaque has several common names. It is often referred to as the long-tailed macaque due to its tail, which is often longer than its body. The name crab-eating macaque refers to its being often seen foraging beaches for crabs. Another common name for M. fascicularis is the cynomolgus monkey, from the name of 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 ἀμέλγειν, amelgein 'to milk' (adj. amolg-os), by claiming that they milked female dogs. This name is commonly used in laboratory settings.
Taxonomy
The 10 subspecies of Macaca fascicularis are:
- Common long-tailed macaque, Macaca fascicularis fascicularis;
- Burmese long-tailed macaque, Macaca fascicularis aurea;
- Nicobar long-tailed macaque, Macaca fascicularis umbrosa;
- Dark-crowned long-tailed macaque, Macaca fascicularis atriceps;
- Con Song long-tailed macaque, Macaca fascicularis condorensis;
- Simeulue long-tailed macaque, Macaca fascicularis fusca;
- Lasia long-tailed macaque, Macaca fascicularis lasiae;
- Maratua long-tailed macaque, Macaca fascicularis tua;
- Kemujan long-tailed macaque, Macaca fascicularis karimondjawae;
- Philippine long-tailed macaque, Macaca fascicularis philippensis.
Characteristics
The body length of the adult, which varies among subspecies, is 38–55 cm (15–22 in) with relatively short arms and legs. Males are considerably larger than females, weighing 5–9 kg (11–20 lb) compared to the 3–6 kg (6.6–13.2 lb) of females. The tail is longer than the body, typically 40–65 cm (16–26 in), which is used for balance when they jump distances up to 5 m (16 ft). The upper parts of the 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 the midline. Their skin is black on their feet and ears, whereas the skin on the muzzle is a light grayish pink color. The eyelids often have prominent white markings and sometimes there are white spots on the 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.
Distribution and habitat
The crab-eating macaque's native range encompasses most of mainland Southeast Asia, from extreme southeastern Bangladesh south 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.
Introduced range
The crab-eating macaque is an introduced alien species in several countries, including Hong Kong, Taiwan, West Papua, Papua New Guinea, New Britain, New Ireland, New Caledonia, Solomon Islands, Fiji, Tonga, Samoa, Nauru, Vanuatu, Pohnpei, Anggaur Island in Palau, and Mauritius. This has led the Invasive Species Specialist Group of the International Union for Conservation of Nature to list the crab-eating macaque as one of the "100 of the World's Worst Invasive Alien Species". In Mauritius, it is a threat for the endemic and endangered Roussea simplex, as it destroys its flowers. It also hinders germination of some endemic trees by destroying most of their fruits when unripe and competes with the endemic endangered Mauritian flying fox for native fruits.
Where it is not a native species, particularly on island ecosystems whose species often evolved in isolation from large predators, it is a documented threat to many native species. The immunovaccine porcine zona pellucida (PZP), which causes infertility in females, is currently being tested in Hong Kong to investigate its use as potential population control.
Behavior and ecology
Macaques live in social groups that contain three to 20 females, their offspring, and one or many males. The groups usually have fewer males than females. In social groups of macaques, a clear dominance hierarchy is seen 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 around 10 years of age and completely stop bearing young by age 24.
The social groups of macaques are female-bonded, meaning the males will disperse at the time of puberty. Thus, group relatedness on average appears to be lower than compared to matrilines. More difference in relatedness occurs 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, male dominance rankings also exist. 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, a decreased value is 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.
Crab-eating macaques sometimes form mixed species groups with other primate species, including the southern pig-tailed macaque, dusky langur and white-thighed surili. They have been observed engaging in grooming with other primate species, including the southern pig-tailed macaque and leaf monkeys such as Raffles' banded langur and the dusty langur.
Reproduction
After a gestation period of 162–193 days, the female gives birth to one infant. The infant's weight at birth is about 320 g (11 oz). 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. 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 sometimes kill infants not their own in order to shorten interbirth intervals. High-ranking females will sometimes kidnap the infants of lower-ranking females. These kidnappings can result in the death of the infants, as the other female is usually not lactating. A young juvenile stays mainly with its 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, though, stay with the group and become incorporated into the matriline into which they were born.
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.
Diet
Despite its name, the crab-eating macaque typically does not consume crabs; rather, it is an opportunistic omnivore, eating a variety of animals and plants. Although fruits and seeds make up 60 - 90% of its diet, it also eat leaves, flowers, roots, and bark. It sometimes preys on vertebrates including bird chicks, nesting female birds, lizards, frogs, and fish, invertebrates, and bird eggs. In Indonesia, it has become a proficient swimmer and diver for crabs and other crustaceans in mangrove swamps. In Bukit Timah, Singapore its diet consists of 44% fruit, 27% animal matter, 15% flowers and other plant matter, and 14% food provided by humans.
The crab-eating macaque exhibits particularly low tolerance for swallowing seeds. Despite its inability to digest seeds, many primates of similar size swallow large seeds, up to 25 mm (0.98 in), and simply defecate them whole. The crab-eating macaque, though, 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. It also can help the plants by distributing seeds to new areas: Crab-eating macaques eat durians such as Durio graveolens and D. zibethinus, and are a major seed disperser for the latter species.
Although the crab-eating macaque is ecologically well-adapted and poses no threat to population stability of prey species in its native range, in areas where it is not native, it can pose a substantial threat to biodiversity. Some believe the crab-eating macaque is responsible for the extinction of forest birds by threatening critical breeding areas as well as eating the eggs and chicks of endangered forest birds.
The crab-eating macaque can become a synanthrope, living off human resources. It feeds 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, it frequently takes food from garbage cans and refuse piles. It can become unafraid of humans in these conditions, which can lead to macaques directly taking food from people, both passively and aggressively.
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 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 and Palau, they are sold as pets. Macaques feed on sugarcane and other crops, affecting agriculture and livelihoods, and can be aggressive towards humans. Macaques may carry potentially fatal human diseases, including herpes B virus. In Singapore, they have adapted into the urban environment.
The macaques have also developed a reputation for actively stealing items from humans (cameras, eyeglasses, hats, etc.), then refusing to return their stolen goods until given food in return. This unique form of kleptoparasitism (known as "robbing and bartering") has primarily been observed in smaller groups of macaques living near Hindu temples and tourist-heavy areas, suggesting it is a learned behaviour within social groups, in response to realizing that humans would trade food for their possessions back.
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 endangered, and CITES lists them as Appendix II. The species' IUCN status was changed in the summer of 2022 from the Least Concern classification in 2020 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. A 2008 review of their populations suggested a need for better monitoring of populations due to increased wild trade and rising levels of human-macaque conflict, which continue to decrease overall population levels despite the species' wide distribution.
Each subspecies faces differing levels of threats, and too little information is available on some subspecies to assess their conditions. The Macaca fascicularis 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 (Macaca fascicularis philippensis) is listed as near threatened, and Macaca fascicularis condorensis is vulnerable. All other subspecies are listed as data deficient and need further study; although recent work is showing Macaca fascicularis aurea and Macaca fascicularis karimondjawae need increased protection. One concern for conservation is, in areas where Macaca fascicularis is not native, their populations need to be monitored and managed to reduce their impact on native flora and fauna.
