tamarin monkey (Saguinus mystax) and the saddle-back tamarin monkey ... KEY WORDS: foraging; computer modeling; tamarin monkeys; Saguinus; spatial ...
International Journal of Primatology, Vol. 14, No. 6, 1993
Modeling Monkeys: A Comparison of Computer-Generated and Naturally Occurring Foraging Patterns in Two Species of Neotropical Primates P. A. G a r b e r 1,3 a n d B. H a n n o n 2 Received March 2, 1992; accepted May 11, 1992
We present a series o f computer-generated foraging models (random movement, olfactory navigation, and spatial memory) designed to examine the manner in which sensory cues and cognitive skills might be used by rainforest monkeys to locate patchily distributed feeding sites. These simulations are compared with data collected in the Amazon Basin of northeastern Peru on the foraging patterns of two species of neotropical primates, the moustached tamarin monkey (Saguinus mystax) and the saddle-back tamarin monkey (Saguinus fuscicollis). The results indicate that, although tamarins may rely on olfactory cues to locate nearby feeding sites, their foraging patterns are better explained by an ability to maintain a detailed spatial map of the location and distribution of hundreds of feeding trees in their home range. There is evidence that such information is retained for a period of at least several weeks and is used to minimize the distance traveled between widely scattered feeding sites. The use o f computer simulations provides a powerful research tool for generating predictive models regarding the role of memory and sensory cues in animal foraging patterns. KEY WORDS: foraging; computer modeling; tamarin monkeys; Saguinus; spatial memory; olfaction.
1Department of Anthropology, University of Illinois, Urbana, Illinois 61801. ZDepartment of Geography, University of Illinois, Urbana, Illinois 61801. Zl'o whom correspondence should be addressed. 827
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INTRODUCTION We present a series of foraging models designed to examine the manner in which sensory cues and cognitive skills might be used by rainforest monkeys to locate widely scattered and ephemeral feeding sites. For species exploiting open habitats, vision may serve as a primary mechanism to select and to navigate between sources of fruit, nectar, leaves, and other plant material. Anthropoid primates are characterized by excellent visual acuity, stereopsis, and color discrimination (Martin, 1990). Evolutionary changes in the primate visual system undoubtedly have had an important effect on patterns of foraging, social communication, and predator detection. But, in arboreal primates, physical constraints imposed by the denseness of the forest canopy may limit the effectiveness of visual cues beyond a distance of some 10-15 m. Given the scattered and patchy distribution of many tropical tree and liana species, nonvisual mechanisms such as olfaction and spatial mapping may play an important role in locating distant or hidden feeding sites (Milton, 1981, 1998; Garber, 1989). Olfaction
The ability to detect and to respond to spatial-temporal differences in odor strengths is highly developed in many groups of higher vertebrates (Moulton, 1967; Epple and Moulton, 1978; Hladik, 1979; Mills, 1989). For example, mammals typically possess two distinct olfactory systems (Estes, 1972): the vomeronasal organ, which lies at the base of the nasal septum and functions principally in the perception of social and sexual odors, and the main olfactory system (olfactory bulb), which is developmentally and functionally independent of the vomeronasal organ (Estes, 1972; Keverne, 1979) and plays a primary role in detecting environmental odors produced by soils, vegetation, and other animal species. The direct association of the olfactory bulb, thalamus, and neocortex in the frontal region of the skull suggests that smells may be encoded with other sensory information and stored as part of experiential memory (Keverne, 1979). Little is known about the ways in which olfactory information is used by animals to make foraging decisions and the degree to which certain species use spatial-olfactory maps to locate feeding sites (i.e., odor cue triggers a memory of the location of a feeding site, or odor trails are followed to reach a feeding site). This lack of specific information results from the difficulties involved in directly measuring odor strengths over large distances as well as in devising natural experiments that eliminate vision, hearing,
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and memory in locating resources. However, just as the physical characteristics of a plant, such as color and size, serve to attract visually oriented foragers, floral scents and the smell of ripe and rotting fruit can provide a chemical signal advertising location and crop availability to olfactory-oriented foragers (Janzen, 1983). Given the importance that odor might play in attracting agents of pollination and seed dispersal, plant fragrances are expected to "have characteristics allowing them to be recognized over long distances under nocturnal weather conditions, distinguished from the multitude of odours in nature, followed through vegetation and other generators or air turbulence" (Janzen, 1983, p. 112).
Evidence for Olfactory Foraging in Primates Marked reduction in the size of the olfactory apparatus in higher primates, especially humans (Martin, 1973; Jensen et al., 1979), has generally been regarded as evidence for limited olfactory capabilities for all primates. However, a species-by-species comparison within the order indicates that certain forms such as the aye-aye, dwarf galago, potto, and mouse lemur maintain a relatively large olfactory bulb, while many leafeating taxa such as the indri, howler monkey, colobus monkey, and gorilla are characterized by greater olfactory reduction than their closely related fruit-eating relatives (Stephan and Andy, 1969). Given the progressive trend in primates for both a decrease in the olfactory bulb and an increase in the size of the neocortex, however, functional interpretations of sensory abilities based solely on measures of brain size must be viewed with caution (Jerison, 1979). A n a t o m i c a l structures for smell are well developed in many prosimians, and there is suggestive evidence that some species use odor cues to locate prey. For example, Charles-Dominique (1977) reports that an African lorisid, the potto (Perodicticus potto), can locate insect prey concealed at a distance of 1 m. Similarly, Hladik (1979) notes that the slender Loris (Loris tardigradus) and the slow Loris (Nycticebus coucang) forage for insects by sniffing the surface of the branch while traveling slowly. In this regard Hladik (1979, p. 327) states, "The unpleasant smell of many invertebrate species, which is generally an antipredator device, is used by L. tardigradus to improve foraging efficiency." The aye-aye (Daubentonia madagascariensis) has an extremely large olfactory bulb for a primate, and it is reported to detect hidden invertebrates using both auditory and olfactory cues (Hladik, 1979). Additional evidence for the possible importance of olfaction in primate foraging includes the exploitation of night-opening o d o r i f e r o u s flowers by several species of
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prosimians (Sussman and Raven, 1978) and suggestions by Wright (1985, p. 650) that food choice in the night monkey (Aotus) is influenced by "an acute sense of smell." Memory and Foraging
There is considerable evidence that many species of animals forage in a manner that enables them to avoid revisiting recently exploited feeding sites, and/or efficiently locate new feeding sites (Armstrong et al., 1987; Balda et al., 1987; Baum, 1987). Although such a pattern could occur in the absence of enhanced cognitive skills [see Armstrong et al. (1987) for a discussion of systematic foraging], experimental studies and field data on seed catching birds and rodents indicate that in certain taxa, spatial memory skills are well developed and serve a critical role in foraging (Balda and Turek, 1984; Balda et al., 1987). Although controlled studies are generally lacking in primates, observations of the feeding behavior of monkeys and apes indicate that many species take what appear to be direct routes to sources of fruits and nectar that are hidden or lie far outside their field of view (Menzel, 1973; Altman, 1974; Sigg and Stolba, 1981; Boesch and Boesch, 1984; Robinson, 1986; Garber, 1988a, 1989). Explanations to account for these goal-oriented foraging patterns have focused principally on cognitive map formation and an ability to integrate information on the amount, location, and availability of potential feeding sites. These explanations are supported by experimental evidence indicating that higher primates exhibit enhanced learning capacities and problem-solving skills (Meador et al., 1986). In perhaps the most clearly documented example, Menzel (1973) had demonstrated that captive chimpanzees not only retain precise spatial information regarding the location of concealed food sources, but also travel to these sites using a distance minimizing foraging route. However, in the absence of predictive models for testing the importance of spatial mapping, odor, and other sensory cues in resource location, conclusions regarding cognitive skills in many primate taxa remain unsubstantiated. The Problem
We investigated the kinds of information that free-ranging tamarin monkeys use to make foraging decisions by comparing actual foraging routes taken with those generated by computer modeling. Tamarins are diurnal, arboreal New World primates that exploit a variety of food resources, including insects, ripe fruit, plant gums, and floral nectar. These
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small monkeys (adult body weight ranges, between 300 and 650 g) maintain a number of functioning scent glands, a vomeronasal organ, and an olfactory bulb that, although smaller than that found in most prosimians, is relatively well developed for a higher primate (Hershkovitz, 1977). Garber (1989, 1993) collected data on the feeding behavior of a mixed species troop of moustached (Saguinus mystax) and saddle-back (Saguinus fuscicollis) tamarins during a 12-month field study in the Amazon Basin of northeastern Peru. These troops are extremely stable, with individuals of each species feeding, foraging, traveling, and resting together throughout the entire year. In order to examine questions regarding foraging and ranging patterns, we collected data every 2 min (point sample) on the feeding behavior and location of members of one of the two resident species from the time individuals exited the sleeping tree in the morning until they entered the sleeping tree in the late afternoon. We also recorded the location of the group in relation to the nearest of 1315 mapped reference points (trees or trail markers) in the troop's home range. Using these data, we were able to map locomotor pathways, to calculate rates of travel, and to record sequential changes in the selection of feeding sites (Garber, 1988a,b). We calculated the distance traveled between feeding sites as the sum distance of each 2-min step. During the course of each day, moustached and saddle-back tamarins traveled approximately 2000 m and fed on the fruit, flowers, or exudates (gums and saps) of 12 trees. The linear or straight-line distance between feeding sites visited successively averaged 92 + 23 m. Both tamarin species exhibit an overall foraging pattern in which (a) daily feeding efforts were generally concentrated on a large number of individual trees (four to eight) from a small number of target species (one or two), (b) trees of the same species were frequently visited in succession, and (c) the nearest tree of a target species (but not the nearest tree in fruit) was generally selected as the next feeding site. Traveling rates during foraging average 5-7 m/min, and the majority of feeding trees had crowns between 5 and 15 m in diameter. In order to compare the foraging routes taken by the tamarins with those expected based on a variety of foraging models, we calculated an index of circuity (CI). Circuity is a measure of the distance actually traveled; divided by the straight-line distance between the starting point and the crown of the next feeding tree. Despite discontinuities in the canopy, and detours necessitated by the presence of streams, dead branches, and the dangers of potential predators, foraging routes taken by the tamarins were relatively direct and averaged 15m (circuity index = 1.19, based on 201 sample feeding bouts) over the straight-line route.
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We can imagine three basic strategies that they might use to find foods that lie outside their immediate visual field. First, they might move randomly or systematically about the forest until an appropriate feeding site comes into view. Second, they might form mental maps of the nearripened fruit they pass and remember these locations relative to their current position in the canopy and/or to particular landmarks. This would require a high degree of spatial memory and an ability to maintain detailed and updated information ot the distribution of particular plant species in their home range. Third, they could track their food by odor. The latter strategy would require a remembered repertoire of familiar odors (overripe, ripe, and near-ripe fruit and flowers of target species) and a well-developed ability to integrate information on odor strength and spatial position for a period of minutes in order to determine the direction of greatest odor concentration. Odor tracking could occur near or far from the feeding site. Combinations of these three basic strategies are also possible.
The Computer Model
We laid out a horizontal plane, 25 m above the ground, which runs through the canopy of all trees, and divided it into cells of unit width and length. We assumed that the monkeys and their food resources are in this plane. X measures the distance from the origin in the center of the space and Y measures the distance perpendicular to X. The odor strength is measured at a point perpendicular to the horizontal X - Y plane. Changes in odor concentration along the X - Y plane were calculated using a pure diffusion model and a diffusion combined with wind effects model (Appendices A and B). The tamarin group is considered a point in this X - Y plane. The group moves in a straight line at a constant 2-m "step" distance. At the end of this "step," a new assessment is made and a new direction of travel is chosen (depending on the model, either by generating a random angle or by a strategy based on comparison of odor concentrations). This process is continued until the group is within sighting distance of a fruiting tree (_ .51), the circuity index was significantly higher (t = 3.56, p
