Natural History of the Black-handed Spider Monkey (Ateles geoffroyi)

by Iris Broekema, November 2002

a young adult female black handed spider monkey, Ateles geoffroyi

Status

Ateles geoffroyi has the critically endangered to endangered status according to The Conservation Union IUCN. The status varies depending on sub species. The IUCN defines the classifications critically endangered as a taxon that it is facing an extremely high risk of extinction in the wild in the immediate future. The classification endangered is defined when it is not critically endangered, but is facing a very high risk of extinction in the wild in the near future. (IUCN, 2002).  The population of spider monkeys in the Azuero penninsula are particularly endangered

Countries of existence

The habitat of Ateles geoffroyi ranges from Mexico to Panama. (Rowe, 1996).

Distinguishing characteristics

The coat color of black-handed spider monkeys varies from light buff to black, depending on the subspecies. The hands and feet are usually black. Infants are born black but in some subspecies the body color lightens appreciably during the first five months. (Rowe, 1996).

Physical characteristics

Table 1: Physical characteristics shows the values of the different parameters for physical characteristics of Ateles geoffroyi.

Table 1: Physical characteristics

Head and body length

305-630 mm (Rowe, 1996).

Tail length

635-840 mm (Rowe, 1996).

Weight

Males: 7420-9000 g (Rowe, 1996), Females: 6000-8912 g (Rowe, 1996).

Intermembral index

105 (Rowe, 1996).

Adult brain weight

110.9 g (Rowe, 1996).

Habitat

Ateles geoffroyi lives in evergreen rain forest, semideciduous forest and mangrove forest. (Rowe, 1996). Spider monkeys are primarily arboreal (adapted to live in trees) and never come to the ground. Ateles is primarily an animal of the upper levels of the forest, with 17.8% of the first sightings in emergents (more than 30m) and 54.5% in the upper part of the canopy (15-20m). The middle levels of the forest were less frequently used, with 19.8% of the first sightings in the middle part of the canopy (20-25m) and only 7.1% in the lower part of the canopy (15-20m).  The species very rarely entered the understory and was seen there only 0.8% of first sightings. Ateles prefers undisturbed high forest. However, in areas where such habitat is limited in extent and where hunting pressure is light or non-existent, and other primate competitors are few in number, it appears to be able to survive in several other forest types as well. Ateles geoffroyi seem to be more flexible in choice of habitat than most of the South American relatives. (Mittermeier, 1988).  We have found that individuals who have been raised in captivity learn to walk on the ground and frequently do so.  In addition, those that have been caged for long periods of time, such as those we obtained from the Fort Sherman Environmental Training Center may take many months to learn to spend much time in the upper levels of the canopy.

Diet

All Ateles species are primarily frugivorous and feed largely on the mature, soft parts of a wide variety of fruits. Other plant parts, particularly young leaves, flowers, bark and decaying wood are eaten less frequently. Spider monkeys supplement their diet with young seeds, floral buds, flowers, flush leaves, pseudobulbs, aerial roots, bark, decaying wood and honey. Ateles eat insects, insect larvae and bird's eggs. Apart from actively feeding on insects, spider monkeys passively ingested insects, such as the larvae of pollinating and parasitic wasps. (Mittermeier, 1988). The diet of Ateles geoffroyi consist of 77.7% of fruit, 11.1% seeds, 9.8% flowers, 7.3% young leaves, 2.6% buds, 1.2% mature leaves and 1.2% animal prey. (Rowe, 1996).

Spider monkeys frequently ingest large qualities of fruits within relatively brief periods of time. Estimates of the importance of fruit in the diet of Ateles range from 82.9-90%. Fruits pass rather quickly through the digestive tract of spider monkeys and the seeds, together with the undigested material, are excreted within a few hours. Frugivory in spider monkeys is characterized most strikingly by the fact that they swallow the seeds of the fruit rather than discard them. In general, fruits are found at or near the periphery of tree crowns. Spider monkeys tend to feed by suspension (hanging, climbing, or moving below tree branches (Rowe, 1996)), and are seldom seen picking a fruit and carrying it away before consuming. Fruits are picked with one hand. A few cases of manipulation have been observed in spider monkeys feeding on fruit. This may be related to the lack of a functional thumb. When fruits are very small or compound, spider monkeys may eat them after picking the whole infructescence or part of it, holding it with the hand(s) and snapping off the fruitlets directly with the mouth. Some fruits are only used for the juice which is obtained by chewing, or only the soft outer layer is scraped off with the teeth. Manipulation of fruit parts with particulate fingers has rarely been observed. Pods are ripped open with the teeth along the suture(s) and eaten out, the hands holding both halves. At maturity, the fruit opens easily by pressure and, after pulling the valves apart with the hands or with hand and teeth, the monkey swallows both seed and aril. When predating on young seeds, spider monkeys bite out part of the fruit-wall until the seed(s) can be eaten. In order to reach some food, spider monkeys have been observed pulling up several meters of stem while sitting on a branch. The leaves selected exclusively for food were young, and as with flowers, they were usually found at the periphery of the tree crown. Flowers were mostly eaten whole, but some species were selected only for the tips of stamens, style and or stigma, or for the sticky central body of staminodes, the honeycup or the thickened perianth. In bark eating, the trunk or the underside of boughs, which were obviously affected by the regular flow of rain water, were most often selected. The preferred patches were quite hard to reach, requiring much effort by the monkeys. Bark was eaten by biting off pieces with the teeth, gnawing for a while and ingesting the pulpy mass. (Mittermeier, 1988).

Groups of spider monkeys split up in subgroups when food resources, are scarce. (Rowe, 1996). The social structure of Atelles seem highly efficient for exploiting the available mature fruit sources, especially since other group members can rapidly learn about these food sources through conspecific cueing. When a foraging subgroup was relatively large, consisting of four or more independently locomoting animals, the monkeys tended to spread their attention across different food sources at any one time, while the leading female, exploited the food source primarily determining the forage route. This type of foraging only seems to be possible when food supply is high, and consequently the presence of one or more food sources nearby is likely. during the long wet season, when this condition is fulfilled, the average subgroup size is larger than during the rest of the year. (Mittermeier, 1988).

Life development

Table 2: Live development shows the values of the different parameters to indicate the life development of Ateles geoffroyi.

Table 2: Live development

Infant

0-24 months (Rowe, 1996).

Sexual maturity

Males: 60 months (Rowe, 1996), Females: 48-60 months (Rowe, 1996).

Estrus cycle

26 days (Rowe, 1996).

Gestation

226-232 days (Rowe, 1996).

Age of first birth 60-90 months (Rowe, 1996).
Duration of milk dependency 2 years (Milton, 1981).

Birth interval

17-45 months (Rowe, 1996).

Life span

27 years (Rowe, 1996).

During early infancy, the infant is continuously carried by the mother, clinging to the mother's ventrum. At about five months of age, Ateles geoffroyi infants tend to ride on the mother’s back. Ateles geoffroyi newborns are entirely black and the reddish pattern on the dorsum does not begin to manifest itself until about five months of age. This feature then defines a transition to the infant-2 class. Only at the end of infancy is full adult coloration attained. Infants usually locomote independently during group progression, but remain with the mother and are still nursed. (Mittermeier, 1988).

Juvenile-2 animals are 24-36 months old and are able to keep up with a fast moving subgroup. They are never observed riding on the mother’s back and gap-bridging by the mother is very rare. Juvenile males show an increasing affiliation with subadults and adult males. Juvenile-3 animals are 36-50 months of age, and stay with the mother most of the time. They play mainly with juveniles of about the same age or with adults. Juvenile-3 animals were often observed taking the initiative in leaving a food source and traveling in front of a subgroup in some parts of the route. They also start to participate in male long-calling and develop their own long call by trial and error. Subadult males are 50 to about 65 months of age. Their body size is almost equal to that of adults, but subadults are less robust. They can also be distinguished from adults by their face color and pigmentation and by a denser fur. They play and wrestle with juveniles more frequently than adults. Female subadults stay almost permanently with the mother even after the mother has given birth to an infant. Subadult males, however, do not from prolonged association with the mother and infant and seem to range independently from the mother. (Mittermeier, 1988).

Locomotion

Ateles locomotion can be divided into five patterns on the basis of limb usage: quadrupedal (using four limbs for locomotion (Rowe, 1996)), walking and running, suspensory locomotion (hanging, climbing, or moving below tree branches (Rowe, 1996)), climbing, bipedalism (using only two limbs for locomotion (Rowe, 1996)), and leaping. The first three are commonly used during both travel and feeding, but climbing and, more particularly, 'horizontal climbing' is the most important pattern during feeding. Quadrupedal walking and running are usually employed on stable horizontal or inclined substrates that are free of obstructions. (Mittermeier, 1988).

Suspensory locomotion can be divided into three patterns: brachiation (swinging with arms from one branch to another (Rowe, 1996)), arm swinging, and upside-down quadrupedalism. Brachiation refers to bimanual progression involving extensive arm and trunk rotation between hand holds. It is usually along supports, but is sometimes across them as well. During brachiation, a tail hold is usually, but not always maintained. Arm swinging refers to bimanual progression without extensive arm and trunk rotation. It usually involves a single swing used to pass obstructions, or to cross between parallel supports, but hand-over-hand arm swinging can also be employed to cover short distances. Upside-down quadrupedalism is rare in adults, but is commonly used by playing juveniles. (Mittermeier, 1988).

Climbing includes a variety of locomotion patterns: quadrupedal climbing, shinnying, descent, horizontal climbing, bridging, supported bipedal walking, pull-ups, lowering, scooting, and swinging. Leaping is used for progression between discontinuous supports. Leaps may be upward, in a horizontal plane or downward, and as a rule takeoffs are from large stable supports. (Mittermeier, 1988).

The most frequent used travel patterns are quadupedal walking and running, suspensory locomotion and climbing. Ateles geoffroyi climbs and leaps more than other spider monkeys. The most frequently used feeding patterns are climbing, suspensory locomotion, and quadrupedal locomotion. Leaping is less important in feeding than in travel, and bipedalism is almost entirely absent. 'Horizontal climbing' is very important during feeding activities in the twigs and branches at the periphery of tree crowns. (Mittermeier, 1988).

Locomotion during travel takes place mainly on branches, with twigs next in importance and boughs third. During feeding, branches play much the same role as in travel, but twigs are much more important and boughs far less. Quadrupedalism and suspensory locomotion take place most often on branches, but twigs are at least as important as branches in many climbing activities. Leaping takes place on all substrates but twigs are more important as landing sites than as takeoff sites. (Mittermeier, 1988).

Ateles feeding posture can be divided into three major categories: sitting, standing and suspensory. Sitting and standing postures are above branch, with the animal's weight resting on the support. Suspensory postures are those in which the major support is above or to the side. Suspensory and sitting postures are the most important feeding, and bipedal, tripedal and quadrupedal standing postures are used only about 10-15% of the time. Reclining and vertical clinging feeding postures are very rare. The majority of both suspensory and sitting feeding postures take place on twigs. Branches are quite important, but boughs play only a minor role. Suspensory postures usually involve three limbs as supports. Four limb and two limb postures show a distant second and third place. Both five limb and one limb postures are rare. (Mittermeier, 1988).

Short resting postures (less than 30 sec duration) are mainly sitting, standing and suspensory, with suspensory postures the most important. The majority are on branches rather than on twigs. Boughs play a minor role. Three limb postures are most often used, but two limb postures are close behind and play a greater role in short resting than in feeding. Long resting postures (more than, or 30 sec duration) are almost entirely sitting or reclining. (Mittermeier, 1988).

The hand of Ateles is prehensile (able to grasp by wrapping around (Rowe, 1996)), and the thumb is vestigial or absent. The hook grip is the main prehensile function of the hand. A kind of precision grip may be performed, which is achieved by scissor-like action of the digits. The tail is prehensile too. (Mittermeier, 1988).

Social Structure

Fission-fusion communities. The ratio of males to females in a community is 1:1.8. (Rowe, 1996). Spider monkeys live in medium-sized, loosely associated groups which fragment into subgroups of varying size and composition, and roam independently in the same general area. The only persistent association is that of a female with her offspring. (Mittermeier, 1988). Overlap of neighboring Ateles groups is 20 to 30%. (Robinson & Janson, 1987). Different parameters can be used to determine the social structure of geoffroyi. Group size, population density, home range, day range, and sleeping sites of Ateles geoffroyi are described below.

Group size

Spider monkeys are usually seen in small groupings of variable size and composition. Spider monkeys live in small temporary subgroups of unstable composition, which form social groups or communities of up to 30 individuals that roam in the same general area. Subgroup size of Ateles geoffroyi ranged from 1 to 20 or more, with an average of about 4.5. (Mittermeier, 1988).

The social system of spider monkeys seems to have evolved in parallel with the species' food specialization, which is particularly directed towards nutritious, large-seeded fruits. The supply of this type of food varies strongly with the seasons, and fruit ripening in general slow and asynchronous within and between individual fruiting plants. Moreover, ripe fruits of this type are available to the monkey only for short periods of time. After ripping, most fruits soon drop to the ground or, when dehiscent, become available to birds. these food plants seldom offer enough to make a visit worthwhile in terms of energy expenditure for more than three independently locomoting spider monkeys. Consequently, subgroups consisting of three or less individuals are most frequent. The high densities of particular food plants fruiting during the long wet season, however, make foraging in much larger subgroups feasible. These can consist of up to nine independently locomoting individuals. During the long dry season, when nutritious fruits are scare, the mean subgroup size decreases sharply, mainly as a result of the splitting of leading-female core areas, which show almost no overlap. These particular females usually lead subgroups within their core areas, and each appears to possess the best ecological knowledge of this area. Throughout the year, males and non-leading females may assemble into subgroups led by such a female in order to share her ecological knowledge of food sources, but during the period of food scarcity they do so less frequently. At the end of the long dry season, when preferred fruit is still in low supply, relatively frequent feeding upon flush leaves and flowers again sustains foraging in larger subgroups, because of the large quality of food offers simultaneously in most large-crowned flushing or flowering plants. (Mittermeier, 1988).

Population density

Ateles geoffroyi has a population density of 6-9 individuals/kmē. (Mittermeier, 1988).

Home range

Ateles geoffroyi has a home range of 1.00-1.15 sq.km. (Mittermeier, 1988). Home range size varies with gender. Males have the largest territories. Females with infants have smaller territories. (Rowe, 1996).

Day range

Ateles geoffroyi has an upper day range of 3000m (Mittermeier, 1988), which rely on ripe fruits, a patchally distributed resource. (Robinson & Janson, 1987).

Sleeping sites

Spider monkeys use many sleeping trees during the year, but only a few are important throughout the year. Spider monkeys seem to select a sleeping tree using several criteria. The tree has to be a tall emergent, which the crown completely free from the canopy beneath. The monkeys prefer a broad, open crown, either small-leafed, leafless or in early flush. The crown has to be more or less horizontally branched; the monkeys seem to refer horizontally forked branches for prolonged resting postures. The tree has to be located strategically with respect to the foraging grounds of the late afternoon and the early morning of the day. The monkeys seem to be very hungry after awaking and prefer to have one or more important food sources near the sleeping tree. A sleeping tree that provides the monkey with a source of food may be given priority. This may be in the form of fruits, flowers or flush leaves of the tree itself, or from epiphytes and/or lianas growing in its crown. Predators at night seems to be the only reasonable explanation for their choice of sleeping trees fulfilling the first three criteria. All subgroup members, except infants, are usually scattered over a sleeping tree crown, with a preference for the center and upper part, and always on branches. By using slender perches in open and isolated crowns, the monkeys would be readily awakened by a felid or other predator climbing the tree. (Mittermeier, 1988).

Behavior

Diurnal and arboreal. Female black-handed spider monkeys seek out trees with large amounts of fruit per visitor to minimize the cost of searching for food. Males spend less time feeding at each site and travel farther, thus increasing their charges of encountering different females. (Rowe, 1996). Parameters for behavior, including activity pattern, relationships among Ateles geoffroyi, communication, and relationships among other animals are discussed below. 

Activity budget

Ateles geoffroyi spent about 54%resting, 27.6% travelling, 10.8% feeding, 6.9% on interaction, and 0.41% on vocalization. (Rowe, 1996).

Relationships among Ateles geoffroyi

Within a social group network of Ateles, certain females can be recognized a leading a subgroup and determining the daily itineraries and activity patterns of the subgroup as a whole. The females usually leave a sleeping tree first, they travel in front of the subgroup most of the time, always feed on the food sources that determine the route that is taken, and initiate most activity patterns. They appear to possess the best knowledge of available food sources within the core area they occupy. The routes taken by a leading female seem to be planned in advance, highly economically and differ greatly from day to day. They consist of the shortest possible connections between consecutive food sources. By contrast, males or non-leading females seem to be incapable of planning an economic route along a large number of relevant food sources, without making loops and without using certain important and well-known food sources repeatedly. Knowledge of available food sources and their exact locations appeared to be restricted to these leading females, and this resulted in a less varied diet, that was mainly composed of foods from particular food sources well-known to most or all members of a group. For males and non-leading females, therefore, it would appear to be advantageous to regularly join subgroups led by such a female in order to learn, through nonspecific cueing, about food sources available at the time. (Mittermeier, 1988).

Female Ateles geoffroyi tend to concentrate their feeding on resources yielding large amounts of food per visit. Females reduce the number of visits to individual trees when the number of available fruits declined, which was not true of the males which used trees over wider areas and visited them more frequently. Females are minimizing their search costs by using few trees offering large amounts of fruit, and that the males, not under the same physiological constrains, are able to minimize the time spent at each site and travel more widely, thereby increasing their changes of contact with different females. (Mittermeier, 1988).

When meeting one another after a period of separation, male spider monkeys belonging to the same group perform a kind of greeting ceremony composed of mutual embracing and pectoral sniffing usually followed by mutual sniffing of the scrotum. Greeting behavior among males invariably appeared to be initiated by the lower-ranking male, and it may be regarded as appeasement behavior. It seems that dominance relationships among spider monkey males are largely determined by age. (Mittermeier, 1988). Conflicts typically begin with males calling, often accompanied by one or more females. Aggression is rare, but adult males can be clearly ranked. There are also dominance relations among some females. Adult males are invariably dominant to females, and adult males also exhibit more aggressive behaviors than do females. Males are the most affiliate, both to other males and to adult females. (Robinson & Janson, 1987).

Adult males were never observed outside the perimeter of the group’s range, and they ranges almost entirely within certain core areas. The adult males appeared to prefer joining a subgroup of one or more group members, especially when it contained one or more leading females. The males usually associates with one female of a set. Males are regularly observed visiting each other’s core area.

Adult males cooperate in territorial defense patrols and long-distance agonistic behavior. In this way, spider monkey males seem to be able to defend larger territories, including ranges of several females, than would be possible in a social system with cohesive bisexual groups. In this respect, spider monkey social system shows a striking similarity to that of chimpanzees. (Mittermeier, 1988). Females often visit neighboring groups, especially when they are carrying newborn infants, and young females may emigrate permanently. (Robinson & Janson, 1987).

Communication

Only male spider monkeys perform long calls. On the forest floor, these long calls are audible at a distance of 800-1000m. Above the canopy, long calls can be heard over approximately 2000m. This appears to be sufficient for spider monkeys to hear every intragroup long call. Long calls are easily recognized individually. During the first part of the long dry season, long calls are heard only occasionally. Spacing may be optimal when males keep relatively silent, especially considering the small day ranges and the drastically decreased energy budgets in this period of food scarcity. It is difficult to find subgroups at this time and the same is probably true for individual spider monkeys. The aggregating component of male long-calling behavior is therefore of minimal importance in this season. The decreased energy budget may be explained not only by the decline of overall food supply, but also by the dietary shift, with flush leaves and flowers constituting a much larger part of the diet. Long-calling behavior seems to be more important during more favorable periods, when day ranges are much larger, energy budgets are increased manifold, and the type of food (ripe fruits) makes a quick depletion likely. (Mittermeier, 1988).

The olfactory behavior patterns used as signals in Ateles are chest-rubbing and pectoral sniffing. Rubbing the chest to and from along a branch deposits secretions from the pectoral glands. Several olfactory behavior patterns have been observed in sexual contexts. The hypertrophied clitoris of female spider monkeys is adapted to deposit drops of urine as scent marks. Although primarily a comfort behavior, rubbing of the and general region, usually performed in a semi-sitting posture, may function as scent marking as well. (Mittermeier, 1988).

Loud, low frequency 'ook-ook' calls or rhythmic panting are used in rough play, but may become more agonistic in character in growls or roars. Barking or 'ook-barks' seem to be produced in motivational conflict situations between approach-withdrawal tendencies. Long loud calls appear to have a distance communication function. Clear, long loud calls or 'whoops' or long calls are performed by males only. (Mittermeier, 1988).

In Ateles, several visual signals have been observed in agonistic situations. These visual signals include head shaking, displacement arm and chest scratching, pilo-erection, hopping and bounding, various arm swaying, and branch shaking and dropping. During agonistic displays the tail may be held up and curled at the tip. In aroused situations, male spider monkeys may perform displacement arm or chest scratching. Open mouth with extreme tooth exposure occurs in threat situations; moderate tooth exposure expresses a tendency to fight. Direct eye contact may also be a threatening expression. (Mittermeier, 1988).

Relationships among other animals

Overt relationships between spider monkeys and other primates, such as capuchins (Cebus) have been reported. Polyspecific associations do exist but are limited to solitary ranging animals of other species, in particular Chiropotes satanas, which may temporarily join a spider monkey subgroup. Most other primates appear to avoid interactions with Ateles, particularly in competitive situations. When a traveling subgroup of Ateles crosses the path of other monkeys, overt agonistic interactions rarely take place and the animals ignore each other. (Mittermeier, 1988). As other animals are drawn to the habitat of Ateles, conflicts may escalate to include intense visual and vocal displays by members of both sexes. (Robinson & Janson, 1987).

Many terrestrial mammals, such as agoutis (Dasyprocta), acouchins (Myoprocta), deer (Mazama), peccaries (Tayassu), and birds such as curassows (Crax), trumpeters (Psophia) and even tortoises (Geochelone) were observed visiting the area below fruiting trees occupied by Ateles. They fed on fruits dropped by the movements of the monkeys or predated the seeds. Alarm calls by these animals usually made the spider monkeys very upset and could easily provoke a branch-shaking and branch-breaking aggressive display directed toward the intruder. (Mittermeier, 1988).

Occasional predation, particularly on juvenile spider monkeys, seem to be the only reasonable explanation for the strong selection of sleeping trees. Daytime predation has never been observed. (Mittermeier, 1988). Little Ateles are vulnerable to eagles, larger Ateles are less, however, they make alarm calls to harpy eagles. (Robinson & Janson, 1987).

References

IUCN. (2002). 2002 IUCN Red List of Threatened Species. The IUCN Species Survival Commission. Retrieved from the web 11/12/02, http://www.redlist.org.

Milton, K.. (1981). Estimates of reproductive parameters for free-ranging Ateles geoffroyi. Primates, 22, 574-579.

Mittermeier, R.A. (1988). Ecology and behavior of neotropical primates, 2. Washington, D.C., World Wildlife Fund.

Robinson, J. G. & Janson, C. H. (1987). Capuchins, squirrel monkeys, and Atelines: Socioecological convergence with old world monkeys. Primate societies, Chicago and London: The University of Chicago Press, pp. 69-82.

Rowe, N. (1996). The pictorial guide to the living primates. East Hampton, New York: Pogonias Press.

http://www.speciesconservation.org/projects/Azuero-Spider-Monkey/586 (2011).  Azuero Spider Monkey (Ateles geoffroyi azurensis).