Habitat preferences, diet, feeding strategy and social organization of the black spider monkey (Ateles paniscus paniscus Linnaeus 1758) in Surinam

This study describes habitat choice of the Surinam black spider monkey ( Atelespaniscuspaniscus ) and clarifies complex temporal and spatial effects of food sources on the behaviour of a group of spider monkeys in a 350 ha study area in central Surinam in terms of food category, food plant identity and phenology, and in terms of quantity, density and dispersion of the most important of these food sources. It recognizes the fundamental importance of mature-fruit feeding to spider-monkey foraging strategy and discusses implications of diet to social behaviour, Prom a conservational point of view. this study in essential in emphasizing the extreme vulnerability of the spider monkey to both hunting and habitat destruction, and in providing detailed information on its habitat choice and dietary requirements. so urgently needed in order to assess in a responsible way the mite of areas to protect and the potential of already preposed protected areas. The spider monkey may serve an an important 'indicator' species, reflecting the degree of disturbance of Amazonian tropical rain forests,1,2,3, Among the eight Surinam monkey species, Atelesp . paniscus is the most restricted in habitat. In the Voltzberg region. it occurs exclusively in high forest (92.6%), infrequently enters edge habitats (14.9%) and is found primarily in the upper levels of the canopy and in emergents (72,3%), The understory is rarely used (0.8%), and the lower extreme of its vertical range appears to be 12 meters.Among the seven major forest types available in the Raleighvallen-Voltzberg region, spider monkeys are observed only in high rain forest. mountain savanna forest, pine. swamp forest and riverbank high forest.4. A total of 207 food plant species are used, of which 68.1% trees. Most important families, providing the monkeys with food, are Moraceae and Mimosaceae regarding both the number of food species and the percentage of total feeding records.Atelesp . paniscus is mainly frugivorous. feeding on 171 species of fruit, 33 species of flower and 28 species of leaf. Mature fruit makes up 96% of the total number of fruit feeding records. The occasional feeding on insects (termites and caterpillars) definitively has been ascertained. The average annual food intake in 82.9% fruits. 6,4% flowers, 7.9% flush leaves, 1.7% bark and 1.0% miscellaneous (e.g., rotten palmsheaths, pseudobulbs, aerial roots, honey, insects). The monthly variation in food choice shows a strong correlation with the phenology. During the first part of the long dry season (July - September), a period of low fruit supply. the monkey compensates its diet with relatively high percen tages of both flowers and flush leaves, while during the long wet season (March - June) fruit abundance causes very low percentages of both flowers and flush leaves in the diet. The percentages are strongly determined individually by its supply in relation to the ecological change, but ripe fruits always are preferred above all.Young seeds play a minor overall role in the diet, except during the period May - June, By ingesting large quantities of young needs# rich in protein and fat, during the peak of the long wet season the monkeys seem to stock up on energy for the coming months of food scarcity (July - October).Ateles appeared to play an important role as dispersal agent for may plant species, and for none species it seemed to be the only disperser. Endozoochorical seed dispersal by spider monkeys took place in 138 plant species (accounting for 93,5% of total fruit feeding records), seed dropping was recorded in 10 species (2,7%) and seed predation in 23 species 3.7%).Ateles belongs to the category of 'specialized frugivores', who derive all or most of their supplies of carbohydrate, lipid and protein from fruits. Large-seeded, nutritious fruits &sea to have coevolved with specialized frugivores an their principal dispersal agents, resulting in a greater quality of dispersal than can be aeon in small-seeded, low nutritious fruits dispersed by a wide array of both 'opportunistic' and 'specialized' fruit-eating animals. This coevolutionary pattern (the high nutritive content of the flesh in large-seeded fruits) way be demon strated in families such as Palmae, Burseraceae. Myristicaceae, Sapindaceae, Loxaniaceael Capparaceae, Sapotaceae and Meliaceae, all producing important fruits for spider monkeys. Among 166 plant species producing edible fruits. used by the spider monkeys in the Voltzberg region, about 80% in nutritious and large-seeded. Low-nutritious, small-seeded fruits (especially berries and figs), making up only 20%, were exploited only incidentally on the way from one nutritious fruit source to another, and almost never appeared to influence the daily foraging routes nor ware revisited regularly. These species often produce mass-ripened fruit crops on which the monkeys cannot depend much, The fruiting seasons of the former category, however, in general last relatively long because of wore or lens asynchronous fruit-maturing within and between indivi duals of the species, apparently mince the small number of specialized dispersal agents way be easily overloaded. The competition between these plant species for the high-quality dispersal offered by a small number of dispersers may have evolved in elongated and displaced, but broadly overlapping fruiting seasons as required for the existence of specialized frugivores.5, Foraging behaviour in spider monkeys in differing strikingly with the seasons. During the long wet season, when fruit is abundant, activity budgets are increased resulting in large day ranges (with a maximum of 5.000 meters), prolonged feeding times, short resting times and many food sources (especially mature fruits) exploited daily. Foraging often takes place in relatively large subgroups breaking up and reassembling regularly,, the subparties using partly different food sources but follow ing about similar itineraries.During the long dry season, when fruit supply is low and a food scarcity or even a food shortage way exist. activity budgets are lowered to a minimum. resulting in short day ranges (with a minimum of 500 meters), prolonged resting times and short feeding times (tow relatively long feeding bouts), few food sources exploited daily and diet composition differing in much higher percentages of flowers and flush leaves. Finally, mean subgroup size is decreased strongly.Spider monkeys live in medium-sized groups fragmenting into widely dis persed subgroups of varying composition. Daily itineraries and activity patterns of a subgroup mostly are determined by a so-called dominant (usually aged) female with or without offspring, or sometimes by two dominant females alternately. These females appear to possess the beet knowledge of certain parts of the group's range, the so-called core areas, and are capable of preplanning an economic foraging route for the day along an much as 8 to 30 different food sources. By checking regularly potential food sources on their stage of maturing and using a highly developed spatial and temporal memory, these females are able to incorporate these food sources in their foraging routes just after becoming available. The interval between subsequent visits to a particular food source appears to be species specific. depending on the rate of fruit maturing. In some species the last stage of maturing in going fast, offering the monkeys every day enough ripe fruits to feed on together. Many species, however, are exploited in a 2 days cycle. some in a 5 - 8 days cycle or even more.Spider monkeys appear to select for variety. using on average about 14 different food items daily. making up about a quarter of the average monthly number of food items used, Among these. 3 or 4 food items are most important considering the amount of feeding time and the estimated total weight of food ingested,6, A group of Atelesp . paniscus usually consists of 15 - 20 individuals. although they way never be observed all together at the same place. A group fragments into several subgroups of varying composition, a female with offspring of an age ranging from 0 to about 5 years being the only persistent bond.Sex ratio of adult males to females is 1 : 2(-3). The adult males of a group appear to defend a territory with clearcut boundaries, while fema les sometimes visit neighbouring groups and even may emigrate.Spider-monkey social system is characterized by its flexible grouping behaviour and seems to be coevolved with the species food specialism concerning mainly nutritious. large-seeded fruits. The supply of this type of food is varying strongly with the seasons and maturing within and between individual fruiting plants. in general. is rather slow and asynchronous. Moreover, individual mature fruits of this type are short ly available to the monkey. After becoming mature. most fruits moon drop to the ground or when dehiscent, become available to birds. For more than three large-sized spider monkeys these food plants seldom offer enough to feed on together and to make the visit worthwhile in terms of energy expenditure, Consequently, subgroups consisting of three or lens indi viduals are encountered most often throughout the year. However, the high density of particular food plants fruiting during the long wet season, makes it possible for spider monkeys to forage in much larger sub groups, often containing two dominant females and ranging in size up to 9 individuals, using simultaneously about the same itineraries, but ex ploiting partly different food sources. As a result. during this season intragroup social interactions are more frequent.During the following long dry season. when nutritious fruits are scarce and some years even a severe food shortage may exist, the mean subgroup size decreases strongly. in particular effectuated so by the splitting of dominant-female core areas, which show almost no overlap anymore. Non-dominant females and males still may join subgroups led by a dominant female to share ecological knowledge of food sources. but they do so less frequently. Day ranges drop strikingly and the animals are more silent, both factors contributing to the lower chance of encounter. Activity budgets are decreased, in particular in males and non-dominant females. The better knowledge of available food in dominant females may favour them especially during the long dry season. This may be a reason that dominant females seem more successful in rearing offspring than non-dominant females, and perhaps that mortality in adult males seems higher considering the sex ratio.At the end of the long dry season. when preferred fruit in still low in supply, the relatively frequent feeding on flush leaves and flowers. again, sustains foraging in larger subgroups, because of the great amount of food offered at the same time and by mostly large-crowned, flushing or blooming food plants.Adult males do have core areas, which are larger than dominant-female core areas and even may, combine those of two dominant females.They cooperate in territorial defense patrols and long distance agonism in case of boundary conflicts. In this way, spider-monkey males seem to be able to defend wore females than they should in a social system with cohesive bisexual groups, like in many other primates.Spider-monkey social system in unusual among primates and only shown striking similarities with that of the chimpanzee ( Pantroglodytes ). Both species are largely frugivorous, and show a loose, unstable social structure within distinguishable groups. Subgroup size varies seasonally in relation to food supply and most commonly is small. Individual adults occupy 'core areas' and show capacity for and continual use of a detailed, high developed spatial memory. Also dominance behaviour and sexual behaviour show remarkable similarities between both species.7. The annual home range of the spider-monkey study group in the Voltzberg study area covered 255 hectares, of which 220 hectares offered suitable habitat, Day range size ranged between 500 and 5.000 meters, depending on the subgroup size and composition, the weather, the season and the distribution of particular important food sources. In the Voltzberg region, Atelesp . paniscus occurs at a density of 7,1 individuals per km 2, or 8.2 individuals per km 2when only suitable habitat is considered. Biomass is ranging between 0.4 and 0.5 kg/ha, depending on the home range figure choosen.Ateles does not show polyspecific associations with other sympatric primate species. Some short-term associations observed were due to chance or should probably be regarded as companionship. Associations with terrestrial birds and mammals, however, are frequently observed and way be advantageous for one or both of the participant species. The terrestrial animals focus on the noisy foraging spider monkeys to obtain nutritious fruits and/or seeds immediately after dropping, while alarm calls emitted by fleeing terrestrial animals way benefit the spider monkeys, warning them against possible intruders coming into the area.8. Spider monkeys are extremely vulnerable to hunting and habitat destruction. All over their range they disappear in the face of human entrance. showing little or no adaptability to human intrusion.Emphasizing the important role of specialized frugivores, like spider monkeys, an dispersal agents for many rain forest plants, and the balance between seed disperser. and seed- and seedling predators as they interact with fruits. having a strong impact on structure and composition of primeval tropical rain forest. a suggestion is made to combine interests of both conservationists and exploiters of rain forest treasures in conservational projects, like that of a responsible exploiting of buffer zones surrounding national parks and nature reserves, by increasing density of particular commercially valuable and edible fruit producing trees, and sustaining restricted game cropping of terrestrial seed predators and herbivores, like agoutis, acouchis, peccaries, deer and tapirs.