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NOTES ON THE ECOLOGY AND BEHAVIOR OF THE PYGMY MARMOSET (CEBUELLA PYGMAEA) IN AMAZONIAN COLOMBIA Martin Moynihan INTRODUCTION Tamarins and marmosets are an abundant and success- ful group of New World primates. They are "mon- keys," members of the suborder Anthropoidea, and distinguished by small size and a series of correlated characters. Within this group, the smallest, the pygmy marmosets of the genus (or perhaps subgenus) Cebu- ella, are remarkable for their extreme specialization. They are, in a sense, the culmination of a major evolutionary trend. It is hoped that the following brief account of the known or surmised behavior and ecology of free-living pygmy marmosets in the "wild" may illustrate and explain some of the peculiarities and constraints within which they have to operate. DESCRIPTION The coloration of Cebuella is largely tan grizzled or brindled with black. Although Hershkovitz (1968) con- sidered the pattern to be primitive, it is also immedi- ately functional (see below). There is considerable variation in the tone of the underparts and the boldness of the brindled stripes on the back. Several coloration variants may be adapted to avoid detection against different backgrounds. The existence of such polymorphism may explain why farmers near El Pepino and Rumiyaco believe there are two species of pygmy marmosets. These people are acute observers, but I believe they are mistaken in this particular instance. They say that both types occur in the same places and have the same habits. I have seen individual marmosets of distinctly different ap- pearance in the same groups. HABITAT Cebuella seems to be confined to the upper part of the Amazon valley (Hill, 1957), a lowland tropical environment of generally humid and stable climate (dry seasons are seldom excessive or prolonged). I was able to observe several groups of pygmy marmosets in and around the localities called El Pepino and Rumiyaco, between the towns of Mocoa and Puerto Asis in the Putumayo region of Colombia, during four field trips (September 17-24, 1968; July 4-11, 1969; February 19-23, 1970; August 12-14, 1970). Under natural conditions, the Putumayo region probably would be covered by high and relatively open "monsoon" or "rain" forests. These forests would be interspersed with small patches and strips of low, dense vegetation, thickets, and tangles on poorer soils, in swamps, on rocky outcrops, at treefalls, and in edge habitats along streams and rivers. Under present conditions, the human population of the region is increasing; much of the forest has been cut down; and there is the beginning of a pollution problem, a by-product of the developing petroleum industry. It is not possible to determine the original habitat preferences of pygmy marmosets. They may well have occurred along edges of forests. According to the local 79
80 MOYNIHAN Indians (and also H. LeNestour, personal communica- tion), they can still be found along edges of forests in the more remote and less disturbed parts of the Putumayo. They may also have occurred within climax forests or at least older communities, in association with trees of Parkia sp. (Hernandez-Camacho and Cooper, 1976). However, I did not find them in either situation. At present, all or most of the local marmosets of El Pepino and Rumiyaco have become commensals of man, adapted to some of the results of human ac- tivities, like some American monkeys of other regions (e.g., the tamarin Saguinus geoffroyi in Panamaâsee Moynihan, 1970). They seem most abundant in "hedges," strips and clumps of degraded woods found between pastures and crop fields from which the most economically valuable (tallest) trees have been re- moved by selective cutting and from which many of the larger mammals have been driven by hunting. The local marmosets occur in small groups. Three to six individuals comprised each of the six groups that I could follow closely. In thick vegetation the animals are very difficult to count precisely, since they tend to "string out": but settlers claim to have seen groups of approximately eight or nine individuals. This suggests that the basic social unit is the family, composed of an adult male and female with their young of the year, sometimes with older young of previous years with their own mates and offspring. If so, the social organi- zation of the species is much the same as those of many other marmosets and the ecologically similar or related tamarins. The average size of groups may be smaller in Cebuella than in such tamarins as Saguinus geoffroyi and S. fuscicollis. but the difference is not great and may be due to recent human intervention. Each group of pygmy marmosets has a well-defined and apparently persistent home range, often the whole of an isolated or semi-isolated hedge or patch of scrub, at times several hundred meters long. These home ranges may be territories defended against intruders, but the usual arrangement of hedges and patches is so dispersed that face-to-face encounters between groups must be infrequent. FEEDING HOLES The El Pepino and Rumiyaco marmosets eat a variety of fruits, buds, and insects. Local people catch them by baiting traps with any convenient fruit, even those not native to the area, such as bananas and plantains. The animals also come down to the ground or cleared pasture to catch grasshoppers. To reach the latter, they have been seen running across asphalt highways. This catholic selection of foods is typical of many monkeys. A more distinctive habit of the pygmy marmosets is "sap-sucking." Every family or group of pygmy marmosets has one or more trees in its home range that are riddled with small holes, sometimes hundreds of them (see Fig- ure 1). The majority of the ones that I inspected were roughly circular, approximately 1-1.5 cm (0.4-0.6 in.) in diameter and half as deep. Some holes appeared to be quite new. In these, it was evident that the cut extended through the bark and just down to the next level, presumably the cambium, but no further. Other holes appeared to be old. They were partly filled in by secondary proliferation of new bark, a sort of scar tissue spreading inward from the sides of the cut. The marmosets visit the holes, at least the newer ones, very frequently and repeatedly. They spend hours going from hole to hole, usually staying no more than a few minutes or even seconds at each. When an individual reaches a hole, it puts its face or muzzle down into the cavity and follows this by slight but rapid movements of the head. A human observer watching from the back or side cannot analyze these movements in detail, but they seem to accompany vigorous action of the mouth and jaws, chewing, lick- ing, or sucking. Obviously, the marmosets are getting something FIGURE 1 Pygmy marmosets on a feeding tree.
NOTES ON THE ECOLOGY AND BEHAVIOR OF THE PYGMY MARMOSET 81 from the holes. They may obtain an occasional insect or grub, but there was no accumulation of insects in the holes I inspected. More significantly, the same holes may be visited at very short intervals, and the later visits are not briefer or simpler than the earlier ones. Insect feeding is not a likely explanation of this behav- ior. A more plausible alternative is that they are feeding on the liquids, presumably sap, which can be seen to leak from the cut surfaces. This hypothesis is supported by the findings of sap or plant gum in the stomachs of pygmy marmosets in another area of Amazonian Colombia (Hernandez-Camacho and Cooper, 1976). Considering the time spent in visiting holes, sap would appear to be a major food source for the marmosets. The local people of El Pepino and Rumiyaco believe that the marmosets cut the feeding holes themselves. Hernandez-Camacho has observed some gnawing by marmosets. The fact that existing holes are used frequently and repeatedly indicates that the actual digging or cutting cannot be a very frequent procedure. I never saw a marmoset dig or cut a hole in a tree that was already riddled, but I did see one individual begin a hole in a previously untouched tree. It is conceivable that the marmosets may prefer to gnaw at sites where the bark has already been damaged by other animals, but their finished feeding holes cannot be confused with either the deeper excavations of woodpeckers (e.g., Dryocoups and Campephilus spp.) or the more extensive "stripping" operations of the local pygmy squirrel. I found marmoset feeding holes in several different species of trees, including an Inga (probably /. spec- tabilis), Matisia cordata, and a tree named cedro by the settlers (possibly Cedrela odorata, Perez- Arbelaez, 1956). I did not find (or recognize) holes in trees of Parkia sp., which appear to be favored by Cebuella elsewhere (Hernandez-Camacho and Cooper, 1976) and which may be the original or "natural" source of sap for many animals in less- disturbed conditions. This seems to be another indica- tion that the El Pepino and Rumiyaco marmosets have already made the translation or transferral to an extraneously managed environment. All the holes that I saw were in trees of appre- ciable size, and presumably age, in trunks and large branches, from only a few centimeters to more than 12 m (40 ft) above ground. The lowest holes seemed older, while the higher holes looked progressively younger. The marmosets must begin drilling at the bottom and gradually work upward. I saw one tree that appeared to have been recently attacked. There were only a few holes in the trunk, all below 3 m (10 ft), in spite of the fact that the tree was moderately thick and tall, reaching a total height of approximately 10 m (30 ft). The marmosets also tend to go from bottom to top during single feeding visits. To my knowledge, Cebuella is the first primate to be found to perform such elaborate sap-sucking. Several other species, prosimians as well as monkeys (see, for instance, Charles-Dominique, 1972), are known to eat plant gums. Some have evolved special adaptations of morphology and/or behavior to facilitate obtaining such food, but they apparently do not usually drill for it. A few Callithrix geoffroyi that I observed in the National Zoological Park in Washington, D.C., chewed on dead branches with quite unusual vigor and persistence. All species of Callithrix share with Cebuella the peculiar character of elongated lower incisor teeth, which may be an adaptation to gnawing hard materials. MOVEMENTS Pygmy marmosets are thoroughly diurnal. Like many diurnal and endothermic vertebrates in the tropics, they are more active in the cooler hours of the morn- ings and late afternoons than at midday. It seems that their periods of activity are more prolonged, on the average, than are those of their larger relatives. This is what would be expected of such tiny animals, with their high metabolic and food requirements. Like all the smaller New World primates except Saimiri, pygmy marmosets sleep in tree holes. Their sleeping holes are not in the same trees as their feeding holes. When they are active but not alarmed, their move- ments and locomotory patterns are conventional, reminiscent of such tamarins as Saguinus fuscicollis. They can run along horizontal or diagonal branches as if on the ground, with a galloping gait, yet may walk or pace when advancing slowly on a branch. They can make long and nearly horizontal leaps of a meter or more, but in many circumstances they are also "vertical clingers and leapers" (Napier and Walker, 1967). Even when not visiting feeding holes, they spend much of their time moving up and down tree trunks. They prefer to rest sitting up or clinging to a trunk in a vertical position. (See Figures 1 and 2.) Although pygmy marmosets can become tame in special situations, they seem to be terrified of potential predators, more so than any of their relatives. One group living in a hedge at the side of a highway paid little attention to either human beings or passing traffic, not even the heaviest, noisiest, most brightly painted or illuminated trucks. However, other less- sophisticated individuals in less extremely aberrant circumstances were exceedingly shy and timid. They use many antipredator devices, all of which seem to be
82 MOYNIHAN FIGURE 2 Hostile patterns of pygmy marmosets. designed to avoid attracting the attention of a predator rather than distracting him. Pygmy marmosets do not show the spectacular "mobbing" behavior of many tamarins. Instead, like squirrels they frequently dodge behind trunks and branches. They also have developed several other protective types of locomotion. Some- times they move exceedingly slowly, making the move- ments difficult to detect, as in the case of sloths (Figure 2). More often, they advance in spurts, lizard- like alternations of dashes and frozen immobility. The immobility, however, can only be partial without losing its effectiveness. An alarmed individual may continue to turn its head in all directions, on the lookout for danger, without becoming conspicuous, since the head is so small, often smaller than surround- ing leaves swaying in the wind. The coloration of the species is highly cryptic. When individuals pass from one tree to another, they almost always prefer to take a low route rather than a high one, thus keeping as far away as possible from the canopy and minimizing exposure to flying birds of prey. (Birds of prey tend to become rare in the immediate vicinity of human settle- ments, doubtless another advantage of such areas from the point of view of the marmosets.) SOCIAL BEHAVIOR The intraspecific social reactions of these animals are partly mediated by "displays," behavior patterns that are specialized to convey information. The repertory of Cebuella displays, as shown by captive adult and juvenile individuals studied in the laboratory of the Smithsonian Tropical Research Institute, on Barro Colorado Island, is a modified version of the basic "language" of all New World primates (Moynihan. 1967). It probably is most similar to the corresponding systems of the marmosets of the genus Callithrix (see Epple, 1968, and comments in Moynihan, 1970), but it is far from identical. Some diagnostic features, such as the apparent use of purely "ultrasonic" alarm calls, may be further adaptations to avoid attracting the attention of predators (the higher the frequency, the less penetration of the sound). In the field, pygmy marmosets are very quiet within the range of frequen- cies audible to human ears, by far the quietest of the monkeys with which I am familiar. RELATIONS WITH OTHER SPECIES Pygmy marmosets must compete with many other animals. Competitors for food, and perhaps perching sites, include lizards and many birds, e.g., iguanas, tanagers, saltators, flycatchers, woodpeckers, and woodcreepers. The marmosets do not react to these animals in obvious manners, except for flinching when a bird comes too close. In the artificial hedges, pygmy marmosets are largely segregated from other nonhuman primates. Although there were reports of groups of Saguinus fuscicollis traversing Cebuella ranges, I did not see any contacts between the two species, nor are they likely to be common. S. fuscicollis usually prefers treefalls and tangles within older forests. I might add that I watched fuscicollis and two other tamarins, Callimico goeldii and another form of Saguinus, pos- sibly graellsi, at some length in other areas without seeing a trace of sap-sucking. In the upper Amazon, among the local primates, sap-sucking seems to be a "trick" of marmosets alone. The pygmy marmoset seems to have come to a special arrangement with the local pygmy squirrels, probably Microsciurus (flaviventer?) napi (name from Hernandez-Camacho, personal communication). These squirrels are widespread in the Putumayo. Like some of the tamarins, they prefer deep or old forest, but they are also regular and persistent occupants of second-growth hedges. In hedge-type habitats, they appear to be less common than the marmosets and less clustered (I saw only single individuals and pairs). The home ranges or territories of the squirrels and mar- mosets broadly overlap in some places. However, I never saw any direct encounters between individuals or groups of the two species. Both are abundant
NOTES ON THE ECOLOGY AND BEHAVIOR OF THE PYGMY MARMOSET 83 enough to suggest that this absence of personal contact is not coincidental. Probably some short-term avoid- ance mechanism is involved. The two species can repeatedly occur at exactly the same sites on the same day, but apparently never at exactly the same time. The squirrels may have a varied diet. I watched only one aspect of their feeding behaviorâbark-stripping. They often gnaw or chew off rather long, irregularly shaped, strips of bark and then appear to eat the bark itself. This bark-stripping is pertinent to the marmosets and can lead to remarkable spatial patterning. One graphic pattern was revealed by inspection of a large tree. Inga sp.. near Rumiyaco. The tree split into four equal trunks a meter or so above its base. Three of the trunks were covered with the marks of gnawing by pygmy squirrels. (I saw the animals at work.) Two of these trunks had no pygmy marmoset feeding holes in them; the third had a few holes on the lower part. The fourth trunk was dotted with marmoset holes all over and had only a very few squirrel marks. Obviously, the two species were divid- ing the tree between them. The number of marmoset holes was about as great as usual in a feeding tree of the species. This would suggest that the marmosets had taken what they wanted and left the rest. If the short- term avoidance mechanism is unilateral, this could mean that the squirrels are more likely to keep away from the marmosets than vice versa. The competition between the two species is serious. Neither the drilling of the marmosets nor the stripping of the squirrels is good for the trees on which they are practiced. The actions of each species tends to have detrimental effects upon the other, at least insofar as they damage or impair the chances of survival of an essential or useful food source. The social segregation of the two species, which permits or facilitates their competitive coexistence in the same places, seems to be partly a matter of timing. The local Indians state, and my own observations tend to confirm, that the squirrels remain active in the middle of the day, when the marmosets are resting, and also during rainstorms, when the marmosets often take shelter. PROSPECTS Cebuella faces a dubious future. The recent partial clearing of land by immigrant human settlers appears to have favored marmosets by providing new foods and patches of suitable habitats. Perhaps they are more widely distributed now than in the past. There are other human activities, however, that could prove to be disastrous. The marmosets are subject to intense hunting and collecting pressures. The local people of the Putumayo find them entertaining. There are not many other equally attractive pets that a schoolboy can keep on his wrist or in his shirt pocket. The marmosets proba- bly could withstand pressures of local origin. How- ever, they cannot support in the long run an interna- tional traffic. They are being trapped for sale and export in large numbers with enormous mortality. Official export figures are probably unreliable for animals as small and easy to smuggle casually as pygmy marmosets. Most trapped individuals may die before they can be shipped, but it is my impression that Cebuella is the monkey most commonly hawked about the streets of many cities of the Amazonian region. The trade should not be allowed to continue. It can only be regulated from the receiving, not the forwarding, end. The simplest solution would be to build up breeding stocks in zoos, laboratories, com- pounds, etc., to satisfy whatever demands may exist or develop. If this could be done, the species should survive, even expand and flourish, in the field, as well as in captivity, for a very long time. SUMMARY Cebuella pygmaea is the smallest and one of the most specialized of New World primates. Individuals of the species were observed near El Pepino and Rumiyaco in the Putumayo region of Colombia. There they have become commensals of man. They occur in family groups in hedges between pastures and crop fields. They eat a variety of animal and vegetable foods, but tend to concentrate upon sap-sucking. Many of their other distinctive featuresâlocomotory habits, color, ultrasonic vocalizationsâwould appear to be anti- predator adaptations. Birds of prey probably were their most important predators under natural conditions. They have many competitors. They are usually segre- gated from Microsciurus sp. by a short-term avoidance mechanism. The partial clearing of forest by human settlers has been favorable to them in some ways. Under the present circumstances, however, they are in danger from excessive hunting for the export trade. If this can be controlled, they should continue to flourish indefinitely. ACKNOWLEDGMENTS My debt to many inhabitants of the Putumayo region must be obvious. 1 am particularly grateful to Sr. Jorge Fuerbringer and his family for all kinds of information, advice, and hospitality. Dr. Jorge Hernandez-Camacho was kind enough to share with me some of the data that he has accumulated through his extensive field experience and to check and correct my more tentative identifications.
84 MOYNIHAN REFERENCES Charles-Dominique, P. 1972. Ecologie et vie sociale de Galago demidovii (Fischer 1808; Prosimii). Advances in Ethology; J. Comp. Ethol. Suppl. 9:7^*1. Epple, G. 1968. Comparative studies on vocalizations in marmoset monkeys. Folia Primatol. 8:1-40. Hernandez-Camacho. J., and R. Cooper. 1976. The nonhuman primates of Colombia. This volume. Hershkovitz. P. 1968. Metachromism or the principle of evolution- ary change in mammalian tegumentary colors. Evolution 22:556- 575. Hill, W. C. O. 1957. Primates. III. Pithecoidea, Platyrrhini. Edin- burgh Univ. Press. Moynihan, M. 1967. Comparative aspects of communication in New World primates. In D. Morris, ed. Primate ethology. Weidenfeld and Nicolson. London. Moynihan. M. 1970. Some behavior patterns of Platyrrhine mon- keys. II. Saguinus geoffroyi and some other tamarins. Smithson. Contr. Zool. 28:1-77. Napier, J. R., and A. C. Walker. 1967. Vertical clinging and leapingâa newly recognized category of locomotor behaviour of primates. Folia Primatol. 6:204-219. Perez-Arbelaez, E. 1956. Plantas titiles de Colombia. Camacho Roldan. Bogota.
