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SULAWESI MACAQUES - A LITERATURE REVIEW

Indonesia 

Indonesia is an archipelago of more than 13,000 islands within which are found the greatest diversity of primates in Asia, with more than 30 different species, mainly endemic (MacKinnon 1986a and b; Rosenbaum et al 1998). The region of Wallacea lies across central Indonesia, named after the great naturalist Alfred Wallace, who identified the area where the flora and fauna of Asia and Australia met and mixed (Whitten et al 1987). The island of Sulawesi (formerly Celebes) is located within this biogeographical area, and extends across the equator from 2^oN to 6^oS (Fooden 1969), measuring approximately 800km by 500km, with an area of 159,000 km² (Whitten et al 1987). The natural vegetation is thick evergreen tropical forest turning to cloud forest and sub-alpine vegetation on the mountain peaks (Fooden 1969). The dominant tree species of the Dipterocarpaceae family, found throughout western Indonesia, are almost totally absent (Whitten et al 1987). Sulawesi contains some of the most distinctive mammal fauna in the country, with127 indigenous species, 98% of which are endemic if the bats are excluded (Whitten et al 1987).

Macaques have the largest distribution of any non-human primate, spreading across habitats from 40^oS to 40^oN (Nickelson and Lockard 1978; Evans et al 1999). There are 19 species worldwide, seven of which are endemic to the island of Sulawesi (Fooden 1969). Here they have radiated to become the most abundant large mammal of the forest, with more species than on any other comparable area of land (Sungkawa 1975, cited in Whitten et al 1987; Reed et al 1997; Rosenbaum et al 1998; Kinnaird, WCMC web site). Most authors (Rosenbaum, O’Brien, Kinnaird etc) accept Fooden’s (1969) classification of the Sulawesi macaques into seven allopatric species, with no evidence of gene flow between them. Other suggestions have come from Thorington and Groves (1970), who viewed the chain of different characteristics as a morphocline within a single species, and Groves (1980) who accepted four species by examining the borders between species for evidence of hybridisation or reproductive isolation.

Fooden (1969) placed all the Sulawesi macaques together in one genus, Macaca, rather than splitting them up as had previously been the case, with some of the northern species classified as Cynopithecus, other authors have considered putting the Sulawesi macaques in a genus of their own (Büttikofer 1917 and DeBaux 1929, cited in Fooden 1969).

It is likely that the Sulawesi macaques are descendants of the pig-tailed macaque M. nemestrina found in Sumatra and Borneo. These animals probably reached Sulawesi by rafting or island hopping during the low sea levels of Pleistocene glaciation (Umbgrove 1938, Van Bemmelen 1949 and Van Andel 1967, cited in Fooden 1969; Whitten et al 1987), possibly at two separate locations or times (Evans et al 1999). The ancestor species then radiated out to colonise the whole island in a continuous distribution (Fooden 1969; Whitten et al 1987). A subsequent rise in sea level of only 4 m above the present would form inundations that would isolate the areas in which M. maura, M. tonkeana, M. hecki and M. nigrescens would later evolve. M. ochreata and M. brunnescens would have been divided then as they are now by the narrow straits between northern Buton and the southeast peninsular of Sulawesi. The segregation between M. nigra and M. nigrescens, and M. tonkeana and M. ochreata is unknown, although it could be a biological barrier of unproductive forests on ultrabasic soils in the later case (Whitten et al 1987). These separations would have allowed the populations to evolve in isolation until they were reproductively incompatible (Fooden 1969).

The macaques are found in lowland and hill forest (Mackinnon 1986a), and have been sighted as high as 2000m, but are probably not common above 1500m (Sarasin and Sarasin 1905, cited in Whitten et al 1987). Pythons Python reticulatus and P. molurus are their only predators other than humans, who hunt them as crop-pests over most of the island and occasionally for food (Whitten et al 1987).

Estimates of group size for some of the Sulawesi macaque species are given by Whitten et al (1987 p. 435), who report M. nigra and M. brunnescens occurring in groups of 30+ individuals; M. nigrescens and M. ochreata in groups of 16 and 18 respectively; and M. maura have been recorded in troops of 20-30 individuals (Matsumura 1998). It is clear that group size within and between species can vary considerably, even inside an area (Whitten et al 1987). Access to fruiting trees is likely to have influenced the evolution of large group sizes, rather than predation pressure, known to be low on Sulawesi (Kinnaird, WCMC web site). High macaque densities in particular areas could be due to high densities of fig trees, but other favoured macaque fruiting trees presumably play a part in the relationship (Bismark 1982, cited in Whitten et al 1987).

Much of the fieldwork on Sulawesi macaques has been on the northern crested species M. nigra, which corresponds to the typical macaque model of large female-bonded, multi-male social groups (Chivers 1986; Reed et al 1997). Females tend to outnumber males 4 to 1, with the society centred around female families, while males move away from their natal groups (Whitten et al 1987; Kinnaird, WCMC web site; Matsumura 1998). A similar social structure has been reported for Moor macaques M. maura (Matsumura 1998).

Cyclical oestrus tumescence (swelling of the buttock region after ovulation) is shown by the sexually mature females of all Sulawesi macaques, and some other Catarrhine species (Büttikofer 1917, cited in Fooden 1969). There is no obvious breeding season under wild conditions (Matsumura 1998).

M. nigra males have been reported to operate a ‘linear and transitive dominance hierarchy’ within groups similar to that of other multi-male macaque species (Reed et al 1997). The social system of female M. nigra is thought to be egalitarian (Reed et al 1997), and that of M. maura has been described as linear (Matsumura 1998). Matsumura (1998) has suggested that all the Sulawesi macaque species have egalitarian social systems and show relaxed dominance styles. This means that social interactions tend to be symmetrical, with high social tolerance, much social grooming and positive interaction, and a high frequency of less severe aggressive behaviour and reconciliation. Between group competition will be of more importance to the almost predator free Sulawesi macaques than within group competition, although the relationships between group living females are probably governed by competition for food (Matsumura 1998).

The only Sulawesi macaque activity budget published so far has been for the black crested macaque M.nigra, studied by O’Brien and Kinnaird (1997), who found that it was generally consistent with most other frugivorous primate species. The most significant difference between M. nigra, and other cercopithecines is the lack of seasonal variation, with the average time spent on each activity practically uniform throughout the year, despite the fluctuating environment (O’Brien and Kinnaird 1997).

M.nigra are described as semi-terrestrial primates (Reed et al 1997) spending more than 60% of the day on the ground resting and travelling, activities that are significantly decreased when the macaques are in the trees, during the morning and afternoon periods (O’Brien and Kinnaird 1997). Arboreal primates often exhibit daily rhythms of behaviour involving increases in foraging in the morning and afternoon (O’Brien and Kinnaird 1997). This pattern was adhered to by the Sulawesi crested macaque groups, who moved and foraged for about 60% of the day, although at a more constant rate than has been reported for some other primates (O’Brien and Kinnaird 1997). Foraging takes precedence over social and other activities, and most of the day is concerned with moving between and exploiting ‘widely-dispersed, temporally fluctuating resources’ (O’Brien and Kinnaird 1997). The remaining time was split almost equally between social activities, primarily in the morning, and resting, mainly in the afternoon, with both occurring together around midday. Small juveniles spend less time foraging and resting and more time socialising (O’Brien and Kinnaird 1997).

Although few interventions in agonistic interactions by a third individual were observed in M. maura (Matsumura 1998), more have been noted in M.nigra by Kinnaird (WCMC web site), who suggests that peaceful interventions to disputes may be unique to macaque species. Yawning is a behaviour that seems to have social significance for macaques during agonistic interactions or dominance displays when adult males perform either half- or full yawns (Dixson 1977).

Once again, studies on home range use have only been published for M.nigra, where no relationship was found between group size and home range area, although there was a correlation with month of the year and group identity, and home ranges overlapped one another considerably (O’Brien and Kinnaird 1997). Macaque home ranges generally include one or more sleeping sites, which tend to be tall, emergent trees (Caldecott 1986), often located close to temporary fruit crops to aid resource defence (O’Brien and Kinnaird 1997). Patterns of home range use are dependent on the spatial and temporal distribution of food resources, and the quality of the forest habitat, with primary forest used significantly more than expected (O’Brien and Kinnaird 1997). It is thought that invertebrates are uniformly distributed throughout the habitat, and as such the home range should be large enough to allow sufficient foraging on this scarce but important resource and include adequate fruiting trees during times of low fruit availability (O’Brien and Kinnaird 1997).

M. nigrescens in Dumoga-Bone National Park were found to travel about 850m per day (Bismark 1982, cited in Whitten et al 1987), while a group of M. nigra were estimated to cover approximately 2 miles (O’Brien and Kinnaird 1997). The need to reach foraging areas and patrol territorial boundaries is thought to dictate a relatively constant rate of travel during the day, although a significantly larger distance is covered during the wet season (O’Brien and Kinnaird 1997).

It can be difficult to determine the diet of Sulawesi macaques, as many of the tree species on the island are undescribed (Groves 1980). O’Brien et al (1997) studying M.nigra in north Sulawesi found that fruit formed the largest component of the diet (66% of observed feeding bouts), with more than 145 different species consumed during the study, matching the general macaque description of ‘opportunistic frugivores’ (Chivers 1986). The Moraceae family accounted for 30.4% of the fruit records, with all but one being Ficus species. Dracontomelum dao was the most frequently eaten fruit species (roughly 15%), with individual trees fruiting at different times of the year to give a continuous food supply (Whitten et al 1987). The bulk of the remainder of the diet was made up of invertebrates (31.5% of observed feeding), probably littoral arthropods and molluscs (Fooden 1969). Occasional vertebrate prey were consumed together with small amounts of vegetative material, likely to be young, tender leaves and shoots (Fooden 1969).

Foraging strategies of M. nigra typically involve moving rapidly across the ground, with brief stops in small-crowned fruit trees or to catch invertebrates, then moving into large crowned trees, such as Ficus species, or D. dao, where the whole group forages together. The need to find invertebrates is thought to influence the routes taken between fruit trees by macaque groups during the day (O’Brien and Kinnaird 1997).

Where farmers and macaques occur together, the monkeys often raid crops (e.g. Heinrich 1965, cited in Fooden 1969). There is a risk to the macaques that they will be chased away by farmers and dogs, and may be attacked with stones or captured in traps, so there must be a large incentive for the raids, such as a decrease in available forest fruits (Caldecott 1986).

Sulawesi macaque groups are often accompanied by rainforest birds such as the endemic fairy billed malkoha Phaenicophaeus calyorhynchus and bay coucal Centropus celebensis, who may be exploiting the monkeys as beaters to flush out grasshoppers and other insects (Fooden 1969; Whitten et al 1987).

‘Habitat loss is widely accepted as the greatest single threat to the continued survival of virtually all primate species’ (Mittermeier and Cheney 1987, cited in Rosenbaum et al 1998). And this is indeed the situation in Indonesia, where agriculture, logging, transmigration camps and oil mining all contribute to the loss of primary forest at an astonishing rate (MacKinnon 1986a; Whitten et al 1987; Rosenbaum et al 1998). More than 67% of productive wet lowland forest on Sulawesi was lost over a period of two decades (Whitten et al 1987; O’Brien and Kinnaird 1996).

Transmigration schemes

Indonesia has a large, expanding human population, estimated to be over 200 million in 1995, with an annual growth rate of 1.56% (USA Immigration Central Web Site). People have been spreading out from the overcrowded islands of Java and Bali and opening up new areas of forest since colonial times (MacKinnon 1986a). The modern Indonesian transmigration program is now the largest scheme for voluntary, assisted migration in the world, with more than 6 million already relocated (Indonesian Department of Foreign Affairs 1999). However, the true number is likely to be 2-3 times this amount when unassisted migrants, attracted by the official settlements, are included. Sulawesi is one of the primary destinations for transmigrants from the environmentally degraded islands of Java, Madura, Bali and Lombok, and had an estimated population of 12,522,000 in 1990 (Whitten et al 1987; Indonesian Department of Foreign Affairs 1999; Encarta web site). Despite this, there is still a large amount of forest cover per inhabitant due to the high percentage of land that is too steep for farming; 83% slopes at more than 15% (Whitten et al 1987).

Slash and burn agriculture is a traditional way of life to many people in Sulawesi; crops are grown for a couple of years after which the land is abandoned to become grassland or secondary forest. Very low production forest is usually safe from agriculture, but may be of limited conservation value as it often supports only a few species at low densities (Whitten et al 1987). Clearing the forest for agriculture brings macaques into contact with humans and their crops. They are capable of becoming major pests, especially of corn, and as such may be killed with stones, captured as pets, or harassed until they move away from the area (MacKinnon 1986a; Southwick and Lindberg 1986; Whitten et al 1987; Rosenbaum et al 1998).

Logging

Most of the lowland forest in Indonesia has already been logged (Myers 1984, cited in Rosenbaum et al 1998), as timber used to be the second most important source of foreign revenue after oil (MacKinnon 1986a) and generated more than 95% of the income of Central Sulawesi, which has only limited oil and gas reserves (Whitten et al 1987). In 1984, the country signed the International Tropical Timber Agreement as one of the most significant producers. Commercial logging for export has now ceased to be important, though forests are still felled for local use (Whitten et al 1987; O’Brien and Kinnaird 1996).

A long-term Food and Agriculture Organisation (FAO) National Parks Development program and World Wildlife Fund program have ensured that all major habitat types are covered in the existing and proposed system of national parks and protected areas (MacKinnon 1986b). Unfortunately, protected areas are often not adequately policed so that settlement and logging may continue within their boundaries (Whitten et al 1987).

Certain studies have indicated that some primate species occur at higher population densities in secondary, logged forests than primary forest due to an increase in leaf growth and food resources (Chivers 1974 and Earl 1992, cited in Rosenbaum et al 1998; MacKinnon 1985). In the forests of Sulawesi fruit tree species diversity is likely to decline after logging, and food resources become lower in quality and quantity (Rosenbaum et al 1998). M. nigra occur at significantly lower densities in logged than primary forest, although the large populations that do remain, albeit at lower numbers, show that there is some conservation value in secondary forest (Rosenbaum et al 1998). Behavioural observations of M. nigra living in secondary forest suggest that they travel further, socialise less, and eat less fruit than conspecifics in better quality primary forest with minimal disturbance and canopy-sized trees (O’Brien and Kinnaird 1997; Rosenbaum et al 1998).

Logging tracks allow easy access into forested areas, facilitating conversion to farmland and hunting expeditions (Rosenbaum et al 1998). Sulawesi macaques are only eaten by non-Moslems, the minority of the population over most of the island, except in the north where the religion is predominantly Christian and macaques are hunted as a delicacy (Sarasin 1905, cited in Fooden 1969; MacKinnon 1986a). During long running studies of M. nigra at Tangkoko-Batuangas Nature Reserve, the macaque population has shown a continuous decline, with densities remaining highest in the centre of the reserve, indicating that the decrease is due to hunting either for commercial or subsistence reasons (Rosenbaum et al 1998). Accidental capture may also occur in traps set for other species such as wild pigs (Groves 1980).

Macaques are commonly kept as pets in villages, about 100 are thought to be living in the Dumonga valley alone (MacKinnon 1986a). Conditions are often poor and life spans short (Groves 1980). All species of Sulawesi macaque are protected by law, although not all are ratified by parliament; so while pets can be confiscated, it is unlikely that the owners will be prosecuted, and guidelines are lacking regarding the future of reclaimed individuals, and their part in species conservation (MacKinnon 1986a).

Illegal trade in endangered species is still common, despite the ratification of the Convention on International Trade in Endangered Species of Flora and Fauna (CITES) in 1978, in which all the Sulawesi macaques are listed in appendix II. Since the Indian ban on rhesus macaque M.mulatta exports, Indonesia, Malaysia, the Philippines and Bolivia have taken over the trade in live animals to research laboratories, primarily in the rich west (MacKinnon 1986a).

The Sulawesi macaque species have limited distributions, but they are not all rare, as they can reach very high population densities, for example M. nigra occurs at 3 animals per ha in the Tangkoko reserve, the highest recorded density of any Indonesian macaque species (MacKinnon 1986a). MacKinnon (1986a) has provided estimates of remaining species population sizes, and numbers protected in reserves as well as data on percentage habitat loss and the size of protected areas, with lists of reserves occurring within species ranges.

Despite its limited distribution, M. nigra is one of the best protected of the Sulawesi macaques, with a large percentage of its range conserved, and a thriving captive population in western zoos (MacKinnon 1986b). There is very little information available on M. nigrescens classified as a subspecies by Groves (1980). M. tonkeana appears to be the most common with a large distribution in an area of low human population (Groves 1980), but the smallest percentage of its population is within protected areas. M. hecki, classified as a subspecies of M. tonkeana by Groves (1980), is distinctive and worth conserving in its own right. These two macaques have only small areas of protected forest within their distribution, but large populations throughout, although they are threatened by transmigration schemes and capture for the pet trade (MacKinnon 1986b).

Very little is known about the distribution or conservation status of M. ochreata, as suggested by the IUCN category of ‘data deficient’. M. brunnescens, classified as a subspecies of M. ochreata by Groves (1980) is suffering heavily from habitat loss, with Muna Island almost totally deforested, and Buton losing its forest at a rate of 10% per year in an area relatively heavily populated by transmigrants (T.Coles, personal communication). M. maura is probably the most threatened Sulawesi macaque as it lives in the densely populated southwest region of Sulawesi, has the smallest population overall and the lowest numbers in protected areas (MacKinnon 1986b; Whitten et al 1987).

Some of the Sulawesi macaque species have large captive populations recorded on the International Species Inventory System (ISIS), where member zoos and wildlife parks are listed. There may be groups in captivity that are not recorded, but these are unlikely to be participating in captive breeding programmes. Although M. nigra is widespread in UK zoos, there is no management for genetic diversity and no plans for reintroduction to protected areas in Sulawesi, all of which probably have macaques already present. Captive macaque social groups can be hard to manage genetically as they tend to be dominated by one male, who is able to control all the mating as a consequence of confined conditions. They can also be very aggressive to one another when there is no room to escape (Pers.obs.). The unnatural conditions and social groupings typically found in captivity may inhibit the full display of natural behaviours and affect dominance relationships (Reed et al 1997). Although expressing certain natural behaviours may not be necessary in captivity, it is important to retain them together with cultural skills if a reintroduction is possible in the future (Sutherland 1998).

In the long-term, the cheapest and most effective method of conserving the Sulawesi macaques is to protect their natural habitat, together with other endangered species (Diamond 1985). The WWF and FAO National Parks Development program covered all major habitat types, so conservation should be fairly comprehensive throughout the country, assuming that reserves are protected and managed efficiently (MacKinnon 1986b). Any of the macaque species that do not have at least 10% of their remaining habitat protected, or a population of at least 5,000 animals should be considered endangered. Reserves should be large enough to contain viable populations and maintain genetic diversity. The most threatened species (M. maura, M. hecki, M. ochreata and M. brunnescens) should be monitored within reserves and managed to maintain adequate populations (MacKinnon 1986a). Outside the reserves, serious crop predation should not be expected to be tolerated, Southwick and Lindberg (1986) have suggested that relocations to other areas may be a solution. However conservation in Indonesia is approached, the provision of conservation information to the public is essential (Groves 1980).

Many authors have bemoaned that fact that there is so little published information on the ecology and behaviour of wild Sulawesi macaques (e.g. Groves 1980; MacKinnon 1986a; Whitten et al 1987; Reed et al 1997; Matsumura 1998). There is practically no data on any of the species, with the exception of M.nigra (e.g. O’Brien, Kinnaird, MacKinnon) and M.maura (Matsumura). Several papers on taxonomy (Albrecht 1978; Fooden 1969; Thorington and Groves 1970; Groves 1980), and genetics (e.g. Kawamoto et al 1985; Ciani et al 1989; Fooden and Laydon 1989; all cited in O’Brien et al 1997) have been published, as well as some captive behaviour studies (e.g. Dixson 1977; Thierry 1983).

Because several Sulawesi macaque species are endangered, information on ecology and behaviour is essential for successful conservation management plans to be designed (O’Brien et al 1997). Definition of habitat requirements, minimum areas for conservation, diet, and details of appropriate social and breeding systems is necessary (Sutherland 1998). Any between species differences or similarities that are noted may be of use in the classification of the macaques as separate species, or subspecies (Fooden 1969; Whitten et al 1987).

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