Gibraltar, Nov. 5 - 8, 2003: A summary
Past ecological changes have affected the present distribution of macaque species. There was a gradual fall in temperature from the Miocene period, when the ancestor of present day macaques appeared on the scene, down to the Pleistocene.
The Pleistocene is the period characterised by most drastic change, including habitat fragmentation, refuges, the appearance and disappearance of land bridges, and sea rafting.
Data evidence the presence of ancestral macaques in central Africa 8 million years ago (mya). From there they extended northwards, reaching NW Africa 7 mya, and NE Africa a million years later.
The Gibraltar Strait gave them access to Europe where they were to emigrate between 5 and 3 mya. Their migration eastwards could have taken place down through eastern Europe or from NE Africa. There is evidence of macaque populations in India from 3 mya, and from here their ample extension as far as Indonesia and Japan. It is believed that the last macaques disappeared from southern Spain during the past 100,000 years. (C. Abegg)
Present day methods of molecular genetic analysis have offered new perspectives as to macaque speciation and phylogenetic relationships. The use of maternal, paternal and bi-parental DNA of individuals from all recognised macaque species have made it possible to reconstruct colonization, diversification and speciation.
For example, an apparently rapid evolutionary radiation characterized the Sulawesi group, where both biotic and abiotic factors played a role, a genetic impact of hybridization being mediated by male transfer. It has also made it possible to up-date the phylogeny of the genus.
Paternal DNA testing has shown that M. arctoides and M. sinica are related, but maternal DNA testing relates M. arctoides to the Fascicularis group. It is probable that M. arctoides is a relatively new species resulting from the hybridization of M. sinica Y-DNA and M. fascicularis mtDNA. A current example are the hybrids between M. maura and M. tonkeanna that have the mtDNA of M. maura.
Regarding M. sylvanus in particular, recent genetic studies situate the species in a monophyletic group with Macaca since 5.5 mya, and disprove its relationship with M. silenus.
The evolution of the species within the Macacagenus appears to have been complex and reticulated and not a linear set of bifurcating events. (D. Melnick).
A study on interspecific variations in pelage have led to a hypothetical description of the last common ancestor to the genus: shoulders medium-brown in colour, lighter on legs and ventrum, darker on the crown and lower back; freckled to grey-coloured face; modest whiskers and slight beard; oestrous coloration pastel pink or blue-grey; round, separate ischial callosities horizontally placed; swelling around the anus, and swollen labia; females weighing between 6 to 7 kilos; sexual dimorphism; short to modest tail. This description is very close to the present day species of M. sylvanus and M. nemestrina.
Another interesting hypothesis has to do with tail reduction or loss. From a study of the anogenital swellings of female Sulawesi macaques, the involvement of the tail in oestrous swellings may have been a determining factor in its reduction, and not climatic changes supported by more traditional theories. (F. Froehlich)
Female philopatry and fission:
A characteristic of the Macaque genus is female philopatry. The number of matrilines within a group will depend largely on population density. When the group becomes too large, fission may occur, whereby a matriline will break off from the group and settle in another area.
Some of the circumstances leading up to fission that have been observed are: increase in competition, decrease in female reproductive success, changes in the male hierarchy, decrease in relatedness, loss of group cohesion, and the formation of clusters.
This last circumstance can be frequently seen before fission occurs, that is, there is a clustering of related kin that will remain with the matriline when the separation takes place.
Fission is the only way for a matriline to spread in natural conditions. It favours kin selection, increasing within-group degrees of relatedness, thereby contributing to the genetic structuration of the population. (N. Ménard)
Samples were collected to test genetic variation within and between the Moroccan and Algerian populations to compare the mtDNA analyses with those of the Gibraltar population to establish the origin of the latter. Phylogenetic analyses suggest that the Gibraltar population is formed by three different haplotypes: two from Morocco and one from Algeria. This study has made it possible to confirm the origin of the present-day matrilines inhabiting the different sites on the Upper Rock of Gibraltar.
The Macaque genus is probably one of the most successful among primates. Although its populations are disjunct and its number reduced, some of the species show a high degree of flexibility as to habitat and diet. Although most macaque species are to be found between the Equator and the Tropic of Cancer, 10% of the species live in the temperate zone. The most adaptable ones include M. mulatta, M. fuscata and M. sylvanus.
Environmental factors can greatly influence group size, group composition, home range size, activity budget, and the distribution of food resources. It could be thought that this last factor would be vital in its effect on social behaviour, clumped resources such as fruit trees and insects leading to frequent and intense competition, and a despotic social structure, while an even distribution such as leaves would lead to infrequent, mild competition, and a tolerant social structure.
However, data from a study on the intake of different resources did not completely support this hypothesis. For example, M. mulatta´s diet consisted of 9% fruit, no seeds, 85% leaves, no invertebrates, and 5% other. Their feeding was mainly done on the ground and consisted of leaves and trifolia. On the other hand, a tolerant species such as M. nigra had a diet of 66% fruit, no seeds, 2% leaves, and 31% invertebrates.
As for the Moroccan M. sylvanus, the diet of those inhabiting the deciduous oak forest consisted of 1% fruit, 32% seeds (acorns), 28% leaves, including lichens and herbs, 11% invertebrates, and 28% other. The cedar oak population differed somewhat: 4% fruit, 27% seeds, 48% leaves, 6% invertebrates, and 15% other. From the data available, it would be premature to hypothesize that social behaviour varies according to regional ecological differences. (D. Hill)
Traditional theories talk about group living, competition and aggression. However, modern studies focus on interspecific variations in conflict management, that is, the mechanisms different species use to avoid aggressive escalation and mitigate its negative consequences. These consequences can range from risk of further aggression, decrease in foraging time, to reduction of tolerance around resources.
Mechanisms to increase tolerance before a potential conflict can include allogrooming, triadic male-infant interactions (particularly in Barbary and Thibetan macaques), and dominance-submission signals (silent bared-teeth display, rounded mouth).
In the post-conflict situation, negative consequences can be mitigated by kin-directed redirection and reconciliation, the latter being inversely proportional to kin bias.
However, no evidence was found for unsolicited consolation. Interspecific variation seems to be related to differences in dominance style which, in some cases, could correspond to phylogenetic relationships. (F. Aureli)
Actually, the selective processes and ecological factors that influence the evolution of social systems are not known. The question is if internal constraints define the space of possibilities open to macaques to cope with environmental constraints.
Two real macaque worlds can be envisaged if we take into account 3 variables:
- Conflict asymmetry: unidirectional aggression leads to submission signals, while bidirectional aggression will most likely lead to conciliatory behaviour, due to feelings of anxiety in both opponents.
- Mother protectiveness. This variable will depend on covarying factors such as the degree of kin bias (the lesser the kin bias, the higher reconciliation), the development of affiliative interactions, the meaning of the bared-teeth display, and the patterns of female rank inheritance.
- The amount of alloparental behaviour.
From available data, two different macaque social structures can be constructed:
- An asymmetric structure where conflict asymmetry rates low, mother protectiveness, high, and alloparental behaviour, low. An example would be the strict hierarchical structure of M. mulatta societies.
- A symmetric structure in which conflict asymmetry and alloparental behaviour rate high, and mother protectiveness, low. A permissive social structure of this type would be that of M. tonkeanna or M. nigra.
If social tolerance were to be graded from despotic to tolerant, the Barbary macaque society would classify as having a moderate dominance asymmetry, a relatively low level of nepotism, elaborate conciliatory behaviours, and a high degree of social tolerance.
According to data from comparative studies, Barbary macaque counter-aggression in conflicts reaches a 41.8%, and their reconciliation, a 24%. However, their kin preference rates a 53%, and their peaceful intervention in conflicts, a 10.4%, which is high in comparison with the 8% for M. tonkeanna, or 9% for M. nigra.
It has been seen that the bared-teeth display can be a sign of submission in some species, a sign of affiliation in others, and a sign of both in M. sylvanus.
Other points to be emphasized in relation with this species are frequent alloparental care, relaxed patterns of rank inheritance among females (in contrast with the "youngest ascendancy" pattern in M. mulatta), and the late dispersal of males (two-thirds transfer after 7 years of age while others remain in their natal group).
The ancestral macaque social structure has probably evolved from a tolerant style to a despotic one during the more recent radiation of macaques (examples being the present social structures of M. mulatta and M. fuscata), in which several appeasement behaviours were lost and the societies became more nespotic and hierarchical, thus decreasing social tolerance.
This phylogenetic analysis of the social behaviour of present day macaque species seems to indicate that the patterns of social organisation in M. sylvanus can be taken, in their most part, as ancestral. This should not come as a surprise considering that morphological and molecular evidence point to M. sylvanus as the most ancient offshoot of the genus Macaca. (B. Thierry)
Macaques seem to be limited in their ability to discriminate kin and males do not appear to recognise their offspring. In the majority of macaque societies the relatedness threshold is low and there is no support from relatives. However, this does not hold true for M. sylvanus where support has been observed from grandmothers, aunts and, even, non-kin.
It appears that age proximity can influence social behaviour when the individuals are raised in the same group, and this can be extended to later sexual activity where sexual interactions are preferred with strangers. (A. Paul)
Studies done on infant handling by male macaques have provided the following hypotheses:
- Paternal: they are the sires and the benefit is direct.
- Kin selection: the male is related to the mother and supports her, so the benefit is indirect.
- Care-then-mate: the male uses it as a mating strategy
- Agonistic buffering.
- Coalition formation with other males in the group and with the mother.
- Rank strategy
Recent studies on male-infant dyadic interactions among the Barbary macaques would mainly support hypotheses 2, 3, 5 and 6. Studies done on carrying preferences show that males carry more for multiparous females, and this takes place more often between high-ranking adult males and high-ranking babies.
Moreover, it was found that, on average, males are related to the mother of the preferred infant. However, there is no correlation between rank order and the number of infants sired.
Regarding infant carriage in Barbary macaques, the study concluded that it is a complex, multilevel behaviour based on coalition formations that seem to be important for maintaining rank and that could reflect a mating strategy.
It also seems to be influenced by relatedness to the mother, perhaps facilitating access to the infant. In general, the data suggest that males interact with infants in their own interest and not for altruistic purposes. (R. Küemmerli)
Male reproductive success, besides being a reflection of the male´s own potential, depends on other parameters such as, female group size, duration of the ovarian cycle, number of cycles prior to conception, and cycle overlap between females.
It has been seen that females prefer polyandrous mating and observations support the hypothesis that the fitness benefit derived from it is a reduction in the risk of infanticide.
In order to achieve this they use tactics that include active behavioural escape, long periods of receptivity, unpredictable ovulation, and signals such as exaggerated swellings, and copulation calls. (C. van Schaik)
This evolution of signals used by females to attract males varies among species. In M. sylvanus there are three: sexual swelling, coloration, and copulation calls (CC). The latter probably evolved in time prior to the other two since these would have coincided with the acquisition of colour vision.
Moreover, there are a number of present day species that have no prominent visual signal (PVS) so, perhaps, the reproductive state is actually revealed acoustically, the remaining signals being secondary in importance. Therefore, it is of interest to examine the possible functions of the female CC.
Firstly, it could incite interference by another male and, thereby, provoke male-male competition, providing an indirect means of female choice. It would then confuse paternity and ensure baby-care by reducing intercopulatory intervals (the sperm competition hypothesis).
Playbacks of the female CC showed that male Barbary macaques were able to discriminate between female copulation calls given at different stages of the oestrous cycle. They responded more strongly to those calls given at the time when conception was most likely to occur. (S. Semple)
A more detailed analysis of the Barbary macaque vocal repertoire revealed a highly graded structure within and between call types, but little acoustic dimorphism. Although phylogenetic relationships appear to set the framework for the structure of calls, these being largely genetically controlled, social structure may influence their function and variation between species.
Available data do not support the dichotomy between graded (continuous acoustic variation) and discreet (no intermediates between call types) repertoires as being determined by ecological factors. (J. Fischer)
In a study of the Middle Hill group in Gibraltar, female Barbary macaques displayed prominent anogenital swellings despite their being highly seasonal breeders. All showed from 2 to 3 swelling cycles, including post-conception swellings.
The size of the maximum swelling ranged between 44 to 136 cm2 and was not related to body weight, age or rank. In all cases, ovulation occurred within the period of maximum swelling. Post-conception swellings were to be observed approximately 26 days after ovulation. Males did not seem to distinguish between a non-conceptive copulation, a conceptive copulation or a post-conceptive one. (U. Moehle)
There is also evidence that Macaque males are more attracted to larger swellings and intervene for them. Anogenital swellings may be maintained during pregnancy to stimulate male-female alliances with side effects on social tolerance and to mitigate stress. (J. Dittami)
Among the female population of M. mulatta on Cayo Santiago, it has been observed that access to food affects the age of first birth. 90% of the females have their first baby at four years of age. However, 3 year old females weighing over 5 kilos have become mothers. This obviously affects life-time reproduction.
Turning to male reproductive ecology on Cayo Santiago, where ecological constraints are minimal, competition over access to females would be expected. However, this was not the case. Data did not point to body mass as the cause of variance in reproductive success among adult males, but it did affect relative reproductive output among younger males. It could be a question of good nutrition.
This increases the testosterone level, producing more estrogen with a consequent reddening of the facial skin, thus leading to female choice. It was seen that 10 or 12 babies born on the same day had been sired by the same male and it was never the alpha male. Many offspring were sired by non-troop males with no rank within the group. Females tended to prefer outsiders.
In conclusion, there seems to be no single optimal strategy for male macaques. Their reproductive success is conditioned by the internal and external circumstances of the individual, and determined by the distribution of females. (F. Bercovitch)
Present day distribution:
The Barbary macaque population of Morocco is presently reduced to approximately 10,000 individuals inhabiting the cedar and oak forests of the Middle Atlas, the High Atlas and the Rif Mountains. The Algerian population numbers between three and four thousand distributed between Akfadou, Roc des Singes, Kherrata, and Djurdjura. The semi-free ranging Barbary macaques of Gibraltar are about 200 in number. (L. Modolo)
The Middle Atlas population of Morocco is distributed within 100 linear square kilometres of 16 transects connected by 300 kilometres of road. Over the past ten years the population density count has dropped between 30% and 40%. However, a density count in this habitat is unreliable due to the way in which the macaques make use of space.
Each troop usually has a home range of approximately 2 square kilometres, but movements are unpredictable due to the presence of modern-day predators (humans and dogs). The macaques prefer the cedar trees or rocky cliffs for protection.
The drastic fall in population size over the past years has been due to (1) culling: the macaques are considered pests due to their bark stripping, an alternative for survival when water is scarce. Nevertheless, studies have shown that bark stripping is still high where primate density has greatly decreased, and that the negative ecological impact is being caused by human factors such as underbrush overgrazing by mixed flocks of sheep and goats; and (2) the unconditioned exploitation of resources: the destruction of the forests in this area by excessive logging, cutting for fire wood, etc.
This has directly affected the distribution of the macaque population. In fact, the sex ratio balance and the number of births have been recognised as an indicator of the quality of the forest: ranging from a high density of adult males in the refuge forests and very degraded forests to a balanced sex ratio in intact forests, and a high density female population in degraded forests; the birth rate being inversely proportionate to the number of adult males in the group.
The situation does not predict an optimistic future for the species if immediate measures are not taken to improve forest management and preservation.
(A. Camerio, M. Mouna)
A situation similar to that in Morocco exists in Japan regarding M. fuscata. The number of macaques has decreased drastically due to habitat degradation, human encroachment, eradication as agricultural pests, among other threats.
Since 1998 around 10,000 individuals have been killed. Despite the decrease in population density, the macaque habitat has expanded. This expansion is due to changes in their natural habitat.
The macaques tend to move out towards the edge of the forest. Some troops come in contact with agricultural areas and, though culling occurs to control crop damage, these troops have shown an increase in birth rate and a decrease in infant mortality.
The Wildlife Protection Law was revised in 1999, but is not considered compulsory. In general, scientific data are deficient, programmes are inappropriate, personnel and laboratories are scarce, economic support lacking, and collaboration weak. (Y. Muroyama)
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