The diet of the Barbary macaque consists primarily of plants and insects.[6] Males play an atypical role in rearing young. Because of uncertain paternity, males are integral to raising all infants. Generally, both sexes and all ages contribute inalloparental care of the young.[7] Males live to around 25 years old while females may live up to 30 years.[8]
Skull and brain, as illustrated inGervais'Histoire naturelle des mammifères3d model of skeleton
The Barbary macaque is first described in scientific literature byAristotle in the fourth century BCE workHistory of Animals. He writes of an ape with "arms like a man, only covered with hair", "feet [which] are exceptional in kind ... like large hands", and "a tail as small as small can be, just a sort of indication of a tail". It is likely thatGalen (129–c.216) dissected the Barbary macaque in the second century CE, presuming the internal structure to be the same as a human. Such was the authority of his work, some mistakes he made were not corrected untilAndreas Vesalius (1514–1564) proved otherwise over a thousand years later.[9] The Barbary macaque was included in the groupingSimia byConrad Gessner in his 1551 workHistoria Animalium,[9] a name which he claimed was already in use by the Greeks.[10] Gessner'sSimia was subsequently used as one ofCarl Linnaeus' four primategenera when he publishedSystema Naturae in 1758. Linnaeus proposed thescientific nameSimia sylvanus for the Barbary macaque.[3] During the next 150 years primate taxonomy was subject to great changes and the Barbary macaque was placed in over thirty differenttaxa.[6] The confusion over the use ofSimia became so great that theInternational Commission on Zoological Nomenclature (ICZN)suppressed its use in 1929.[10][6] This meant the Barbary macaque was placed in the next oldest genus assigned to it,Macaca, described byBernard Germain de Lacépède in 1799.[6]
The Barbary macaque is the mostbasal macaque species.[11][12]Phylogenetic andmolecular analyses show it is asister group to all Asian macaque species. The results of a phylogenetic analysis show that the chromosomes of Barbary macaque resemble those of therhesus macaque with the exception of chromosomes 1, 4, 9, and 16. It was also discovered that chromosome 18 in the Barbary macaque ishomologous tochromosome 13 in humans.[6]
Polymerase chain reaction studies have foundAlu element insertions, small pieces of genetic code ingenomes, can infer primate phylogenetic relationships. Using this method the phylogenetic relationship of ten species within the genusMacaca has been resolved, showing the Barbary macaque to be a sister group to all other macaques.[11]
Barbary macaquefossils have been found across Europe, from the Atlantic Ocean to the Black Sea, dating from the EarlyPliocene (earlyZanclean5.3 to 3.6 million years ago[13])to theLate Pleistocene, assigned to various subspecies includingM. s. sylvanus,M. s. pliocena andM. s. florentina.[5] Theinsular dwarfM. majori endemic to Sardinia-Corsica during theEarly Pleistocene, usually considered to have derived from Barbary macaque, is generally considered a distinct species. Remains fromNorfolk, England, dating to theMiddle Pleistocene, at53 degrees latitude, are amongst the northernmost records of non-human primates.[5]Archaic humans and Barbary macaque remains were found co-occurring at numerous sites.[14] It is thought possible that humans consumed Barbary macaques.[15][16] The youngest known remains of a Barbary macaque in Europe were discovered at Hunas in Bavaria, Germany, dated to 85,000–40,000 years ago. The distribution of the Barbary macaque in Europe was likely strongly influenced by climate, only extending into Northern Europe duringinterglacial intervals.[5][17] It was restricted to more southerly regions during colder glacial phases.[18] The disappearance of the Barbary macaque in Europe may have been caused by humans.[19]
Fossils of the Barbary macaque are known from the Guefaït-4.2 site in Morocco, dating to around the Pliocene-Pleistocene boundary approximately 2.6 million years ago where measurements ofcarbon isotopes andoxygen isotopes indicate that the macaque consumed primarily the fresh fruits and leaves ofC3 plants.[20]
The Barbary macaque has a dark pink face with a pale buff to golden brown to grey pelage and a lighter underside. The colour of mature adults changes with ages.[21][6] In adults and subadults the fur on the back is variegated pale and dark which is due to banding on individual hairs. In spring to early summer, as the temperatures rise, the adult macaquesmoult their thick winter fur. The species showssexual dimorphism with males larger than females. The mean head-body length is 55.7 cm (21.9 in) in females and 63.4 cm (25.0 in) in males. The bonelessvestigial tail is greatly reduced compared with other macaque species and, if not absent, measures 4–22 mm (0.16–0.87 in). Males may have a more prominent tail, though data is scarce.[6] The average body weight is 9.9–11 kg (22–24 lb) in females and 14.5–16 kg (32–35 lb) in males.[6][22]
Like all Old World monkeys, the Barbary macaque has well-developed sitting pads (ischial callosities) on its rear.[22] Females exhibit an exaggeratedanogenital swelling,[23][24] which increases in size duringoestrus.[25][26] It has cheek pouches and high-crownedbilophodont molars (molars with two ridges); the third molar is elongated.[22] The diploidchromosome number of the Barbary macaque is 42, like other members of the Old World monkeytribePapionini.[6]
Historically, the Barbary macaque occurred across North Africa from Libya to Morocco.[2] It is the only primate in Africa that survives north of theSahara Desert.[21] It lives mainly infragmented areas of theRif and theMiddle andHigh Atlas mountain ranges inMorocco and theGrande andPetite Kabylie mountain region inAlgeria. It has been recorded at elevations of 400–2,300 m (1,300–7,500 ft), though it seems to prefer higher elevations. The Moroccan and Algerian populations are around 700 km (430 mi) apart, although the gap was smaller during theHolocene.[6]
It can live in a variety of habitats, such ascedar,fir, andoak forests,grasslands,thermophilous scrub, and rocky ridges full of vegetation inMediterranean climate with seasonal extremes of temperature.[6][21] In Morocco, most Barbary macaques inhabitAtlas cedar (Cedrus atlantica) forests, but this could reflect the present habitat availability rather than a specific preference for this habitat.[6] In Algeria, the Barbary macaque inhabits mainly Grande and PetiteKabylia, ranges that form part of theTell Atlas mountain chain, but there is also an isolated population inChréa National Park.[29][2] It lives in mixed cedar andholm oak forests, humidPortuguese andcork oak forests, and scrub-covered gorges.[29]
Fossil evidence indicates that the Barbary macaque occurred in southern Europe during thePleistocene and duringinterglacial periods also in England.[30] A Tunisian population was mentioned in the works of ancient Greek writerHerodotus, indicating the species has become extinct there within the last 2,500 years.[6]
The Barbary macaque is gregarious, forming mixed groups of several females and males. Troops can have 10 to 100 individuals and arematriarchal, with their hierarchy determined bylineage to the lead female.[31] Unlike other macaques, the males participate in rearing the young.[31] Males may spend a considerable amount of time playing with andgrooming infants. In this way, a strong social bond is formed between males and juveniles, both the male's own offspring and those of others in the troop. This may be a result ofselectivity on the part of the females, who may prefer highly parental males.[7]
The mating season runs from November through March. Thegestation period is 147 to 192 days, and females usually have only one offspring per pregnancy. Females rear twins in rare instances. Offspring reach maturity at three to four years of age, and may live for 20 years or more.[32]
Grooming other Barbary macaques leads to lowerstress levels for the individuals that do the grooming.[33] While stress levels do not appear to be reduced in animals that are groomed, grooming more individuals leads to even lower stress levels; this is a benefit that might outweigh the costs to the groomer, which include less time to participate in other activities such as foraging. The mechanism for reducing stress may be explained by the social relationships (and support) that are formed by grooming.[33]
Male Barbary macaques interfere in conflicts and form coalitions with other males, usually with related males rather than with unrelated males. These relationships suggest that males do so in order to indirectly increase their ownfitness. Furthermore, males formcoalitions with closely related kin more often than they do with distantly related kin.[34] These coalitions are not permanent and may change frequently as male ranking within the group changes. Although males are more likely to form coalitions with males who have helped them in the past, this is not as important as relatedness in determining coalitions.[34] Males avoid conflicting with higher ranking males and will more frequently form coalitions with the higher ranking male in a conflict.[34] Close grouping of males occur when infant Barbary macaques are present. Interactions between males are commonly initiated when a male presents an infant macaque to an adult male who is not caring for an infant, or when an unattached male approaches males who are caring for infants. This behaviour leads to a type of social buffering, which reduces the number of antagonistic interactions among males in a group.[31]
An open mouth display by the Barbary macaque is used most commonly by juvenile macaques as a sign of playfulness.[35]
The main purpose of calls in Barbary macaques is to alert other group members to possible dangers such aspredators. Barbary macaques can discriminate calls by individuals in their own group from those by individuals in other groups ofconspecific macaques. Neither genetic variation nor habitat differences are likely causes ofacoustic variation in the calls of different social groups. Instead, minor variations in acoustic structure among groups similar to the vocal accommodation seen in humans are the likely cause. However, acoustic characteristics such aspitch andloudness are varied based on the vocalizations of individuals they associate with, and social situations play a role in the acoustic structure of calls.[36][37]
Barbary macaque females have the ability to recognize their own offspring's calls through a variety of acoustic parameters. Because of this, infant calls do not have to differ dramatically for mothers to be able to recognize their own infant's call. Mothers demonstrate different behaviours on hearing the calls of other infant macaques as opposed to the calls of their own offspring. More parameters for vocalizations lead to more reliable identification of calls in both infants and in adult macaques so it is not surprising that the same acoustic characteristics that are heard in infant calls are also heard in adult calls.[38]
Although Barbary macaques aresexually active at all points during a female's reproductive cycle, male Barbary macaques determine a female's most fertile period bysexual swellings on the female.[39] Mating is most common during a female's most fertile period. The swelling size of the female reaches a maximum around the time of ovulation, suggesting that size helps a male predict when he should mate. This is further supported by the fact that male ejaculation peaks at the same time that femalesexual swelling peaks. Change in female sexual behaviour around the time of ovulation is insufficient to demonstrate to the male that the female is fertile. The swellings, therefore, appear necessary for predicting fertility.[26]
Barbary macaque females differ from other nonhuman primates in that they often mate with a majority of the males in their social group. While females are active in choosing sexual associations, the mating behaviour of macaque social groups is not entirely determined byfemale choice.[39] These multiple matings by females decrease the certainty of paternity of male Barbary macaques and may lead them to care for all infants within the group. For a male to ensure his reproductive success, he must maximize his time spent around the females in the group during theirfertile periods. Injuries to male macaques peak during the fertile period, which points to male-male competition as an important determinant of male reproductive success.[39] Not allowing a female to mate with other males, however, would be costly to the male, since doing so would not allow him to mate with more females.[39]
Closeup of the face of a juvenile in GibraltarA young macaque at the Montagne des Singes,Alsace
Barbary macaques from all age and sex groups participate inalloparental care of infants. Male care of infants has been of particular interest to research because high levels of care from males are uncommon in groups where paternity is highly uncertain. Males even act as true alloparents of infant macaques by carrying them and caring for them for hours at a time as opposed to just demonstrating more casual interactions with the infants. The social status of females plays a role in female alloparental interactions with infants. Higher-ranking females have more interactions, whereas younger, lower-ranking females have less access to infants.[7]
The diet of the Barbary macaque consists of a mixture of plants and insect prey. It consumes a large variety ofgymnosperms andangiosperms. Almost every part of the plant is eaten, including flowers, fruits, seeds, seedlings, leaves, buds, bark, gum, stems, roots, bulbs, and corms. Common prey caught and consumed by Barbary macaques are snails, earthworms, scorpions, spiders, centipedes, millipedes, grasshoppers, termites,water striders,scale insects, beetles, butterflies, moths, ants, and even tadpoles.[6]
Barbary macaques can cause major damage to the trees in their prime habitat, theAtlas cedar forests inMorocco. Since deforestation in Morocco has become a major environmental problem in recent years, research has been conducted to determine the cause of the bark stripping behaviour demonstrated by these macaques. Cedar trees are also vital to this population of Barbary macaques as an area with cedars can support a much higher density of macaques than one without them. A lack of a water source and exclusion of monkeys from water sources are major causes of cedar bark stripping behaviour in Barbary macaques. Density of macaques, however, is less correlated with the behaviour than the other causes considered.[40]
The Barbary macaque's main predators are thedomestic dog,[6]leopard andeagles; thegolden eagle may only prey on cubs, since it is morphologically not adapted to hunt primates.[41] The approach of eagles and domestic dogs is known to elicit analarm call response.[6]
Wild populations of Barbary macaques have suffered a major decline in recent years to the point of being declared anendangered species on theIUCN Red List since 2008. The Barbary macaque is threatened by fragmentation and degradation of forest habitat, andpoaching for the illegal pet trade; it is also killed in retaliation for raiding crops.[2][42]Today, no accurate data exists on the location and number of individuals out of their natural habitat. An unknown number of individuals are living in zoological collections, at other institutions, in private hands, in quarantine, or waiting to be relocated to appropriate destinations.[2]
The habitat of the Barbary macaque is under threat from increasedlogging activity.[43] Local farmers regard the Barbary macaque as pest and engage in its extermination. Once common throughout northern Africa and southern Mediterranean Europe, only an estimated 12,000 to 21,000 Barbary macaques are left in Morocco and Algeria. Once, its distribution was much more extensive, spreading east through Algeria, Tunisia and Libya, and north to the United Kingdom. Its range is no longer continuous, with only isolated areas of range remaining. By thePleistocene, it inhabited the warmer Mediterranean regions of Europe, from theBalearic Islands and mainlandIberia and France in the west, east to Italy,Sicily,Malta, and as far north asGermany and Norfolk in the British Isles.[44]The species decreased with the arrival of the lastLast Glacial Period, going functionally extinct on theIberian Peninsula except for Gibraltar around 30,000 years ago.[45]
The Barbary macaque is threatened byhabitat loss,overgrazing, and illegal capture. In Morocco, tourists interact with Barbary macaques in many regions. Information collected in the interviews with inhabitants in the High Atlas of Morocco indicated that the capture of macaques occurs in these regions. Conflict between local people and wild macaques is one of the greatest challenges to Barbary macaque conservation in Morocco. The main threats to the survival of Barbary macaques in this region have been found to behabitat destruction and the impact of livestock grazing, but problems of conflict with inhabitants are also increasing due to crop raiding and the illegal capture of macaques. Human–macaque conflict is mainly due to crop raiding. In the High Atlas of Morocco, macaques attract a large number of tourists every year, and they are favoured for their potential benefits to tourism. In addition, macaques have some ecological roles; for example, they are the predators of several destructive insects and pests of plants and participate in seed dispersal in many plant species.[46][47][48][49][50][51]
In the Central High Atlas, the Barbary macaque occurs in relatively small and fragmented areas restricted to the main valleys at elevations of 700–2,400 m (2,300–7,900 ft). In a 2013 study, researchers reported that they found Barbary macaques in relatively small and fragmented habitats in 10 sites, and that the species no longer occurred in four localities. This could be attributed to habitat degradation, hunting activities, the impact of livestock grazing, and disturbance by people. As deforestation for agriculture andovergrazing continues, the remaining forest becomes increasingly fragmented. Consequently, the Barbary macaque is now restricted to small, fragmented relict habitats.[46]
Many of the mistaken ideas about humananatomy contained in the writings ofGalen are apparently due to his use of the Barbary macaque, the onlyanthropoid available to him, indissections.[52] Strongculturaltaboos of his time prevented his performing any dissections of humancadavers, even in his role asphysician and teacher of physicians.[53]
Macaques in Morocco are frequently used as photo props, despite their protected status.[54] Tourists are encouraged to take photos with the animals for a fee. Macaques are also sold as pets in Morocco and Algeria, and exported to Europe to be used as pets and fighting monkeys, both in physical marketplaces and online.[54][55]
Tourists interact with wild monkeys across the globe, and in some situations, tourists may be encouraged to feed, photograph, and touch the monkeys. Although tourism has the potential to bring in money towards conservation goals and provides an incentive for the protection of natural habitats, close proximity and interactions with tourists can also have significant psychological impacts on the Barbary macaques. Fecal samples and stress-indicating behaviours, such as belly scratching, indicate that the presence of tourists has a negative impact on the macaques. Human activities such as taking photographs cause the animals stress, possibly because the people come too close to the animals and make prolonged eye contact (a sign of aggression in many primates). Macaques that live in areas close to human contact have more parasites and lower overall health than those that live in wilder environments, at least in part due to the unhealthy diets they receive as a result of feeding from humans.[56][57]
Several groups of Barbary macaques can be found in tourist sites, where they are affected by the presence of visitors providing food to them. Researchers comparing two such groups in the central High Atlas mountains in 2008 found that the tourist group of Barbary macaques spent significantly more time engaged in resting and aggressive behaviour, and foraged and moved significantly less than the wild group. The tourist group spent significantly less time per day feeding on herbs, seeds, and acorns than the wild group. Human food accounted for 26% of the daily feeding records for the tourist group, and 1% for the wild-feeding group.[48]Scientists who collected data on the seasonal activity budget and diet composition of the endangered Barbary macaque group inhabiting a tourist site in Morocco found that activity budgets and diet of the study group varied markedly among seasons and habitats. The percentage of daily time spent in foraging and moving was lowest in spring, and the daily time spent in resting was highest in spring and summer. The time budget devoted to aggressive display was highest in spring than the other three seasons. There is an increase in the daily feeding time spent eating flowers and fruits in summer, seeds, acorns, roots and barks in winter and autumn, herbs in spring and summer, and a clear increase in consumption of the human food in spring.[47]The tourist and the wild groups did not differ in the proportion of daily records devoted to terrestrial feeding, but the tourist group spent a significantly lower percentage of daily records in terrestrial foraging, moving and resting, while performing more terrestrial aggressive displays more than the wild group. There was no significant difference between the two groups in the proportion of terrestrial feeding records spent eating fruits; but the tourist group had lower daily percentages of terrestrial feeding on leaves, seeds and acorns, roots and barks, and herbs, while it spent higher daily percentages of terrestrial feeding on human food.[49]
Barbary macaques were traded or perhaps given as diplomatic gifts as long ago as the Iron Age, as indicated by remains found in such sites asEmain Macha in Ireland, dating to no later than 95 BC; an Iron Age hillfort, theTitelberg in Luxembourg; and two Roman sites in Britain.[58]
^abLinnaeus, C. (1758)."Simia sylvanus".Systema naturæ per regna tria naturæ, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Vol. I (Decima, reformata ed.). Holmiæ: Laurentii Salvii. p. 25.
^Castaños, P.; Murelaga, X.; Arrizabalaga, A.; Iriarte, M.-J. (2011). "First evidence ofMacaca sylvanus (Primates, Cercopithecidae) from the Late Pleistocene of Lezetxiki II cave (Basque Country, Spain)".Journal of Human Evolution.60 (6):816–820.Bibcode:2011JHumE..60..816C.doi:10.1016/j.jhevol.2011.01.011.PMID21481922.
^Alba, D. M.; Carlos Calero, J. A.; Mancheño, M. Á.; Montoya, P.; Morales, J.; Rook, L. (2011). "Fossil remains ofMacaca sylvanus florentina (Cocchi, 1872) (Primates, Cercopithecidae) from the Early Pleistocene of Quibas (Murcia, Spain)".Journal of Human Evolution.61 (6):703–718.Bibcode:2011JHumE..61..703A.doi:10.1016/j.jhevol.2011.09.003.PMID22014683.
^Fidalgo, D.; Rosas, A.; Estalrrich, A.; García-Tabernero, A.; Pastor, F. J.; Pineda, A.; Huguet, R.; Cáceres, I.; Ollé, A.; Vallverdú, J.; Saladie, P. (2023). "First presence ofMacaca sylvanus at the late Early Pleistocene of Barranc de la Boella (La Mina locality, Francolí Basin, NE Iberia)".Journal of Human Evolution.179 103368.Bibcode:2023JHumE.17903368F.doi:10.1016/j.jhevol.2023.103368.hdl:10261/308760.PMID37094515.
^Möhle, U.; Heistermann, M.; Dittami, J.; Reinberg, V.; Hodges, J. K.; Hodges, J. K. (2005). "Patterns of anogenital swelling size and their endocrine correlates during ovulatory cycles and early pregnancy in free-ranging barbary macaques (Macaca sylvanus) of Gibraltar".American Journal of Primatology.66 (4):351–368.doi:10.1002/ajp.20161.PMID16104035.S2CID19899619.
^abBrauch, Katrin; Pfefferle, Dana; Hodges, Keith; Möhle, Ulrike; Fischer, Julia; Heistermann, Michael (2007). "Female sexual behavior and sexual swelling size as potential cues for males to discern the female fertile phase in free-ranging Barbary macaques (Macaca sylvanus) of Gibraltar".Hormones and Behavior.52 (3):375–383.doi:10.1016/j.yhbeh.2007.06.001.PMID17644098.S2CID30650507.
^abcDeag, J. M (1980). "Interactions between males and unweaned Barbary macaques: testing the agonistic buffering hypothesis".Behaviour.75 (1):54–80.doi:10.1163/156853980x00564.
^Kuester, J. (1999). "Male migration in Barbary macaques at Affenberg Salam".International Journal of Primatology.20 (1):85–106.doi:10.1023/A:1020536317646.S2CID43112228.
^Fischer, J.; Hammerschmidt, K. (2002). "An overview of the Barbary macaque,Macaca sylvanus, vocal repertoire".Folia Primatologica.73 (1):32–45.doi:10.1159/000060417.PMID12065939.S2CID9791964.
^Hammerschmidt, K.; Todt, D. (1995). "Individual differences in vocalisations of young Barbary macaques (Macaca sylvanus): a multi-parametric analysis to identify critical cues in acoustic signalling".Behaviour.132 (5):381–399.doi:10.1163/156853995x00621.
^abcdKuester, J.; Paul, Andreas (1992). "Influence of male competition and female mate choice on male mating success in Barbary macaques".Behaviour.120 (3/4):192–216.doi:10.1163/156853992x00606.JSTOR4535008.
^Ciani, A. C.; Camperio, A.; Martinoli, L.; Capiluppi, C.; Arahou, M.; Mouna, M. (2001). "Effects of water availability and habitat quality on barkstripping behavior in Barbary macaques".Conservation Biology.15 (1):259–265.Bibcode:2001ConBi..15..259C.doi:10.1111/j.1523-1739.2001.99019.x.S2CID86080812.
^van Uhm, D. P. (2016). "Monkey business: the illegal trade in Barbary macaques".Journal of Trafficking, Organized Crime and Security.2 (1):36–49.hdl:1874/358227.
^Von Segesser, F.; Menard, N.; Gaci, B.; Martin, R. D. (1999). "Genetic differentiation within and between isolated Algerian subpopulations of Barbary macaques: evidence from microsatellites".Molecular Ecology.8 (3):433–442.doi:10.1046/j.1365-294x.1999.00582.x.PMID10199007.S2CID23657621.
^O'Reagan, H. (2008). "The Iberian Peninsula corridor or cul-de-sac? Mammalian faunal change and possible routes of dispersal in the last 2 million years".Quaternary Science Reviews.27 (23–24):2136–2144.Bibcode:2008QSRv...27.2136O.doi:10.1016/j.quascirev.2008.08.007.
^abEl Alami, A.; Chait, A. (2012). "Seasonal variation in activity budget and diet of the endangeredMacaca sylvanus in the tourist valley of Ouzoud, Central High Atlas, Morocco".Mammalia.76:245–250.doi:10.1515/mammalia-2011-0054.S2CID87795900.
^abEl Alami, A.; Van Lavieren, E.; Aboufatima, R.; Chait, A. (2012). "Differences in activity budgets and diet between semiprovisioned and wild-feeding groups of the endangered Barbary macaque (Macaca sylvanus) in the Central High Atlas Mountains, Morocco".American Journal of Primatology.74 (3):210–216.doi:10.1002/ajp.21989.PMID24006539.S2CID18223816.
^abEl Alami, A.; Chait, A. (2013). "Comparison of the terrestriality of Barbary macaques (Macaca sylvanus) between tourist and wild sites in the region of Ouzoud, Morocco".Mammalia.78 (4):539–542.doi:10.1515/mammalia-2013-0061.S2CID87021869.
^El Alami, A.; Chait, A. (2014). "Distribution of the endangered Barbary macaque and human-macaque interaction in the tourist region of Ouzoud, central High Atlas of Morocco".African Journal of Ecology.53 (3):375–377.doi:10.1111/aje.12191.
^El Alami, A.; Chait, A. (2015). "Roles of tourism in the local people opinion regarding human-macaque conflict in the central High Atlas, Morocco".Revue de Primatologie.7:1–7.
^Ustun, C. (2004). "Galen and his anatomic eponym: vein of Galen".Clinical Anatomy.17 (6):454–457.doi:10.1002/ca.20013.PMID15300863.
.jpg)
