Route-based travel and shared routes in sympatric spider and woolly monkeys: cognitive and evolutionary implications

Many wild primates occupy large home ranges and travel long distances each day. Navigating these ranges to find sufficient food presents a substantial cognitive challenge, but we are still far from understanding either how primates represent spatial information mentally or how they use this information to navigate under natural conditions. In the course of a long-term socioecological study, we investigated and compared the travel paths of sympatric spider monkeys (Ateles belzebuth) and woolly monkeys (Lagothrix poeppigii) in Amazonian Ecuador. During several field seasons spanning an 8-year period, we followed focal individuals or groups of both species continuously for periods of multiple days and mapped their travel paths in detail. We found that both primates typically traveled through their home ranges following repeatedly used paths, or “routes”. Many of these routes were common to both species and were stable across study years. Several important routes appeared to be associated with distinct topographic features (e.g., ridgetops), which may constitute easily recognized landmarks useful for spatial navigation. The majority of all location records for both species fell along or near identified routes, as did most of the trees used for fruit feeding. Our results provide strong support for the idea that both woolly and spider monkey use route-based mental maps similar to those proposed by Poucet (Psychol Rev 100:163–182, 1993). We suggest that rather than remembering the specific locations of thousands of individual feeding trees and their phenological schedules, spider and woolly monkeys could nonetheless forage efficiently by committing to memory a series of route segments that, when followed, bring them into contact with many potential feeding sources for monitoring or visitation. Furthermore, because swallowed and defecated seeds are deposited in greater frequency along routes, the repeated use of particular travel paths over generations could profoundly influence the structure and composition of tropical forests, raising the intriguing possibility that these and other primate frugivores are active participants in constructing their own ecological niches. Building upon the insights of Byrne (Q J Exp Psychol 31:147–154, 1979, Normality and pathology in cognitive functions. Academic, London, pp 239–264, 1982) and Milton (The foraging strategy of howler monkeys: a study in primate economics. Columbia University Press, New York, 1980, On the move: how and why animals travel in groups. University of Chicago Press, Chicago, pp 375–417, 2000), our results highlight the likely general importance of route-based travel in the memory and foraging strategies of nonhuman primates.

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This contribution is part of the Special Issue “A Socioecological Perspective on Primate Cognition” (Cunningham and Janson 2007).     

Children's spatial knowledge of their neighborhood environment

Six-, eight-, and ten-year-olds' spatial knowledge of their neighborhood was examined. Children initially made bearing and distance estimates from their homes to three distant landmarks in the neighborhood area. They were then asked how far their parents permitted them to travel in the neighborhood with freinds and by themselves and how far they actually traveled. Finally, children described how they found their way from one neighborhood location to another. There were three major findings. First, children at all age levels knew the general direction to distant landmarks, suggesting that children as young as 6-years-old can infer spatial relations in large, familiar environment. Second, activity range increased over age, with boys ranging further than girls. Third, although children took advantage of a wide variety of cues to find their way in their neighborhood, clear developmental patterns of cue utilization and ldway-findingrd strategies were not evident.     

How do wild baboons (<Emphasis Type="Italic">Papio ursinus</Emphasis>) plan their routes? Travel among multiple high-quality food sources with inter-group competition

How do humans and animals travel between multiple destinations on a given foraging trip? This question is of theoretical and practical interest, yet few empirical data exist to date. We examined how a group of wild chacma baboons travelled among multiple, simultaneously fruiting mountain fig trees (Ficus glumosa). In the course of a 16-month study, this highly preferred fruit was available during a 3-week period, from relatively few sites, which were also utilized by four larger baboon groups. We used directness of route and travel speed of 13 days of observation, and approach rates of 31 days of observation to differentiate between purposeful and opportunistic encounters with 50 fig trees. The study group visited a total of 30 fig trees overall, but only 8 trees per day on average. Each morning, they travelled along a highly repetitive route on all days of observation, thereby visiting 2–4 fig trees. They approached these trees rapidly along highly directed paths without intermittently exploiting other food sources that were available in large quantities. Then, they abruptly changed behaviour, switching to lower travel speed and less directed routes as they foraged on a variety of foods. They approached additional fig trees later in the day, but approach rates were similar to those at times of year when fruit of this fig species was unavailable; this suggested that encounters with trees after the behavioural switch were not planned. Comparing visits to purposefully and opportunistically encountered trees, we found no difference in the average time spent feeding or frequency of feeding supplants, suggesting that purposefully and opportunistically visited trees had similar values. We conclude that when foraging for mountain fig fruit the baboons’ cognitive maps either contain information on relatively few trees or of only a single route along which several trees are situated, leading to very limited planning abilities.     

Integrating information about location and value of resources by white-faced saki monkeys (<Emphasis Type="Italic">Pithecia pithecia</Emphasis>)

Most studies of spatial memory in primates focus on species that inhabit large home ranges and have dispersed, patchy resources. Researchers assume that primates use memory to minimize distances traveled between resources. We investigated the use of spatial memory in a group of six white-faced sakis (Pithecia pithecia) on 12.8-ha Round Island, Guri Lake, Venezuela during a period of fruit abundance. The sakis’ movements were analyzed with logistic regressions, a predictive computer model and a computer model that simulates movements. We considered all the resources available to the sakis and compared observed distances to predicted distances from a computer model for foragers who know nothing about the location of resources. Surprisingly, the observed distances were four times greater than the predicted distances, suggesting that the sakis passed by a majority of the available fruit trees without feeding. The odds of visiting a food tree, however, were significantly increased if the tree had been visited in the previous 3 days and had more than 100 fruit. The sakis’ preferred resources were highly productive fruit trees, Capparis trees, and trees with water holes. They traveled efficiently to these sites. The sakis choice of feeding sites indicate that they combined knowledge acquired by repeatedly traveling through their home range with ‘what’ and ‘where’ information gained from individual visits to resources. Although the sakis’ foraging choices increased the distance they traveled overall, choosing more valued sites allowed the group to minimize intragroup feeding competition, maintain intergroup dominance over important resources, and monitor the state of resources throughout their home range. The sakis’ foraging decisions appear to have used spatial memory, elements of episodic-like memory and social and nutritional considerations. This contribution is part of the Special Issue “A Socioecological Perspective on Primate Cognition” (Cunningham and Janson 2007).     

What wild primates know about resources: opening up the black box

We present the theoretical and practical difficulties of inferring the cognitive processes involved in spatial movement decisions of primates and other animals based on studies of their foraging behavior in the wild. Because the possible cognitive processes involved in foraging are not known a priori for a given species, some observed spatial movements could be consistent with a large number of processes ranging from simple undirected search processes to strategic goal-oriented travel. Two basic approaches can help to reveal the cognitive processes: (1) experiments designed to test specific mechanisms; (2) comparison of observed movements with predicted ones based on models of hypothesized foraging modes (ideally, quantitative ones). We describe how these two approaches have been applied to evidence for spatial knowledge of resources in primates, and for various hypothesized goals of spatial decisions in primates, reviewing what is now established. We conclude with a synthesis emphasizing what kinds of spatial movement data on unmanipulated primate populations in the wild are most useful in deciphering goal-oriented processes from random processes. Basic to all of these is an estimate of the animal’s ability to detect resources during search. Given knowledge of the animal’s detection ability, there are several observable patterns of resource use incompatible with a pure search process. These patterns include increasing movement speed when approaching versus leaving a resource, increasingly directed movement toward more valuable resources, and directed travel to distant resources from many starting locations. Thus, it should be possible to assess and compare spatial cognition across a variety of primate species and thus trace its ecological and evolutionary correlates. This contribution is part of the special issue “A Socioecological Perspective on Primate Cognition” (Cunningham and Janson 2007b)     

Effects of route traveled on the distance estimates of children and adults

Second graders, sixth graders, and adults walked about an experimental environment containing seven stimulus locations and three large barriers. Each individual learned the environment while traveling along a prescribed route. The environment was constructed such that 12 of the interlocation distances represented the factorial combination of route (traveled vs not traveled), barrier (absent vs present), and distance (4-, 6-, and 8-ft). After criterial performance in learning the environment, each person gave distance estimates of the 12 critical distances. In general, the estimates of the length of routes that were traveled, were long and had no intervening barrier were more accurate than the estimates of the length of routes which were not traveled, were short, and had intervening barriers to prevent direct travel. In addition, for 4- and 6-ft distances, subjects overestimated barrier present paths which were not traveled relative to the other three estimates for each distance (barrier present traveled, barrier absent traveled, barrier absent not traveled). These findings emphasize the generative nature of the construction of spatial representations and suggest that functional distance, or ease of travel, does not influence this construction in a simple manner. Results are discussed in terms of the ability to coordinate spatial information with general knowledge of spatial relationships.     

Gibbon travel paths are goal oriented

Remembering locations of food resources is critical for animal survival. Gibbons are territorial primates which regularly travel through small and stable home ranges in search of preferred, limited and patchily distributed resources (primarily ripe fruit). They are predicted to profit from an ability to memorize the spatial characteristics of their home range and may increase their foraging efficiency by using a ‘cognitive map’ either with Euclidean or with topological properties. We collected ranging and feeding data from 11 gibbon groups (Hylobates lar) to test their navigation skills and to better understand gibbons’ ‘spatial intelligence’. We calculated the locations at which significant travel direction changes occurred using the change-point direction test and found that these locations primarily coincided with preferred fruit sources. Within the limits of biologically realistic visibility distances observed, gibbon travel paths were more efficient in detecting known preferred food sources than a heuristic travel model based on straight travel paths in random directions. Because consecutive travel change-points were far from the gibbons’ sight, planned movement between preferred food sources was the most parsimonious explanation for the observed travel patterns. Gibbon travel appears to connect preferred food sources as expected under the assumption of a good mental representation of the most relevant sources in a large-scale space.     

Experimental evidence for route integration and strategic planning in wild capuchin monkeys

Both in captivity and the wild, primates are found to travel mostly to the nearest available resource, but they may skip over the closest resource and travel to more distant resources, which are often found to be more productive. This study examines the tradeoff between distance and reward in the foraging choices of one group of wild capuchin monkeys (Cebus apella nigritus) using feeding platforms in large-scale foraging experiments conducted over four years. Three feeding sites were arrayed in an oblique triangle, such that once the monkey group had chosen one site to feed, they had a choice between two remaining sites, a close one with less food and the other up to 2.3 times as far away but with more food. Sites were provisioned once per day. The capuchins generally chose the closer feeding site, even when the more distant site offered up to 12 times as much food. The distances to, rewards of, or various profitability measures applied to each alternative site individually did not explain the group’s choices in ways consistent with foraging theory or principles of operant psychology. The group’s site choices were predicted only by comparing efficiency measures of entire foraging pathways: (1) direct travel to the more rewarding distant site, versus (2) the longer ‘detour’ through the closer site on the way to the more distant one. The group chose the detour more often when the reward was larger and the added detour distance shorter. They appeared to be more sensitive to the absolute increase in detour distance than to the relative increase compared to the straight route. The qualitative and quantitative results agree with a simple rule: do not use the detour unless the energy gain from extra food outweighs the energy cost of extra travel. These results suggest that members of this group integrate information on spatial location, reward, and perhaps potential food competition in their choice of multi-site foraging routes, with important implications for social foraging. This contribution is part of the special issue “ A Socioecological Perspective on Primate Cognition” (Cunningham and Janson 2007b).     

The importance of gesture in children's spatial reasoning

On average, men outperform women on mental rotation tasks. Even boys as young as 4 1/2 perform better than girls on simplified spatial transformation tasks. The goal of our study was to explore ways of improving 5-year-olds' performance on a spatial transformation task and to examine the strategies children use to solve this task. We found that boys performed better than girls before training and that both boys and girls improved with training, whether they were given explicit instruction or just practice. Regardless of training condition, the more children gestured about moving the pieces when asked to explain how they solved the spatial transformation task, the better they performed on the task, with boys gesturing about movement significantly more (and performing better) than girls. Gesture thus provides useful information about children's spatial strategies, raising the possibility that gesture training may be particularly effective in improving children's mental rotation skills.     

Aiming error under transformed spatial mappings suggests a structure for visual-motor maps

Transformed spatial mappings were used to perturb normal visual-motor processes and reveal the structure of internal spatial representations used by the motor control system. In a 2-D discrete aiming task performed under rotated visual-motor mappings, the pattern of spatial movement error was the same for all Ss: peak error between 90 degrees and 135 degrees of rotation and low error for 180 degrees rotation. A two-component spatial representation, based on oriented bidirectional movement axes plus direction of travel along such axes, is hypothesized. Observed reversals of movement direction under rotations greater than 90 degrees are consistent with the hypothesized structure. Aiming error under reflections, unlike rotations, depended on direction of movement relative to the axis of reflection (see Cunningham & Pavel, in press). Reaction time and movement time effects were observed, but a speed-accuracy tradeoff was found only for rotations for which the direction-reversal strategy could be used. Finally, adaptation to rotation operates at all target locations equally but does not alter the relative difficulty of different rotations. Structural properties of the representation are invariant under learning.     

Spatial working memory for clustered and linear configurations of sites in a virtual reality foraging task

Two experiments using an immersive virtual reality foraging environment determined the spatial strategies spontaneously deployed by people in a foraging task and the effects on immediate serial recall of trajectories though the foraging space, which could conform or violate specific organisational constraints. People benefitted from the use of organised search patterns when attempting to monitor their travel though either a clustered "patchy" space or a matrix of locations. The results are discussed within a comparative framework.     

Spider monkey ranging patterns in Mexican subtropical forest: do travel routes reflect planning?

Although it is well known that frugivorous spider monkeys (Ateles geoffroyi yucatanensis) occupy large home ranges, travelling long distances to reach highly productive resources, little is known of how they move between feeding sites. A 11 month study of spider monkey ranging patterns was carried out at the Otochma’ax Yetel Kooh reserve, Yucatán, Mexico. We followed single individuals for as long as possible each day and recorded the routes travelled with the help of a GPS (Global Positioning System) device; the 11 independently moving individuals of a group were targeted as focal subjects. Travel paths were composed of highly linear segments, each typically ending at a place where some resource was exploited. Linearity of segments did not differ between individuals, and most of the highly linear paths that led to food resources were much longer than the estimate visibility in the woodland canopy. Monkeys do not generally continue in the same ranging direction after exploiting a resource: travel paths are likely to deviate at the site of resource exploitation rather than between such sites. However, during the harshest months of the year consecutive route segments were more likely to retain the same direction of overall movement. Together, these findings suggest that while moving between feeding sites, spider monkeys use spatial memory to guide travel, and even plan more than one resource site in advance. This contribution is part of the special issue “A Socioecological Perspective on Primate Cognition” (Cunningham and Janson 2007).     

Three-dimensional spatial representation in freely swimming fish

Research on spatial cognition has focused on how animals encode the horizontal component of space. However, most animals travel vertically within their environments, particularly those that fly or swim. Pelagic fish move with six degrees of freedom and must integrate these components to navigate accurately--how do they do this? Using an assay based on associative learning of the vertical and horizontal components of space within a rotating Y-maze, we found that fish (Astyanax fasciatus) learned and remembered information from both horizontal and vertical axes when they were presented either separately or as an integrated three-dimensional unit. When information from the two components conflicted, the fish used the previously learned vertical information in preference to the horizontal. This not only demonstrates that the horizontal and vertical components are stored separately in the fishes' representation of space (simplifying the problem of 3D navigation), but also suggests that the vertical axis contains particularly salient spatial cues--presumably including hydrostatic pressure. To explore this latter possibility, we developed a physical theoretical model that shows how fish could determine their absolute depth using pressure. We next considered full volumetric spatial cognition. Astyanax were trained to swim towards a reward in a Y-maze that could be rotated, before the arms were removed during probe trials. The subjects were tracked in three dimensions as they swam freely through the surrounding cubic tank. The results revealed that fish are able to accurately encode metric information in a volume, and that the error accrued in the horizontal and vertical axes whilst swimming in probe trials was similar. Together, these experiments demonstrate that unlike in surface-bound rats, the vertical component of the representation of space is vitally important to fishes. We hypothesise that the representation of space in the brain of vertebrates could ultimately be shaped by the number of the degrees of freedom of movement that binds the navigating animal.     

Three-dimensional spatial representation in freely swimming fish

Research on spatial cognition has focused on how animals encode the horizontal component of space. However, most animals travel vertically within their environments, particularly those that fly or swim. Pelagic fish move with six degrees of freedom and must integrate these components to navigate accurately—how do they do this? Using an assay based on associative learning of the vertical and horizontal components of space within a rotating Y-maze, we found that fish (Astyanax fasciatus) learned and remembered information from both horizontal and vertical axes when they were presented either separately or as an integrated three-dimensional unit. When information from the two components conflicted, the fish used the previously learned vertical information in preference to the horizontal. This not only demonstrates that the horizontal and vertical components are stored separately in the fishes’ representation of space (simplifying the problem of 3D navigation), but also suggests that the vertical axis contains particularly salient spatial cues—presumably including hydrostatic pressure. To explore this latter possibility, we developed a physical theoretical model that shows how fish could determine their absolute depth using pressure. We next considered full volumetric spatial cognition. Astyanax were trained to swim towards a reward in a Y-maze that could be rotated, before the arms were removed during probe trials. The subjects were tracked in three dimensions as they swam freely through the surrounding cubic tank. The results revealed that fish are able to accurately encode metric information in a volume, and that the error accrued in the horizontal and vertical axes whilst swimming in probe trials was similar. Together, these experiments demonstrate that unlike in surface-bound rats, the vertical component of the representation of space is vitally important to fishes. We hypothesise that the representation of space in the brain of vertebrates could ultimately be shaped by the number of the degrees of freedom of movement that binds the navigating animal.     

Rhesus monkeys (<Emphasis Type="Italic">Macaca mulatta</Emphasis>) remember agency information from past events and integrate this knowledge with spatial and temporal features in working memory

The purpose of the present study was to examine whether rhesus monkeys remember information about their own agency—along with spatial, temporal and contextual properties—from a previously experienced event. In Experiment 1, rhesus monkeys (n = 4) used symbols to reliably indicate whether they had performed or observed an event on a computer screen. In Experiment 2, naïve and experienced monkeys (n = 8) reported agency information when stringent controls for perceptual and proprioceptive cues were included. In Experiment 3, five of the monkeys completed a task in which they reported agency information along with spatial and temporal features of events. Two monkeys performed this agency discrimination when they could not anticipate which memory test they would receive. There was also evidence that these features were integrated in memory. Implications of this research are discussed in relation to working memory, episodic memory and self-awareness in nonhuman animals.     

Comparing Locomotion With Lever-press Travel In An Operant Simulation Of Foraging

An operant model of foraging was studied. Rats searched for food by pressing on the left lever, the patch, which provided one, two, or eight reinforcers before extinction (i.e., zero reinforcers). Obtaining each reinforcer lowered the probability of receiving another reinforcer, simulating patch depletion. Rats traveled to another patch by pressing the right lever, which restored reinforcer availability to the left lever. Travel requirement changed by varying the probability of reset for presses on the right lever; in one condition, additional locomotion was required. That is, rats ran 260 cm from the left to the right lever, made one response on the right lever, and ran back to a fresh patch on the left lever. Another condition added three hurdles to the 260-cm path. The lever-pressing and simple locomotion conditions generated equivalent travel times. Adding the hurdles produced longer times in patches than did the lever-pressing and simple locomotion requirements. The results contradict some models of optimal foraging but are in keeping with McNair's (1982) optimal giving-up time model and add to the growing body of evidence that different environments may produce different foraging strategies.     

Visual discrimination,sequential learning and memory retrieval in the Australian desert ant <Emphasis Type="Italic">Melophorus bagoti</Emphasis>

Bees, wasps and ants—so-called central-place foragers—need potent homing strategies to return to their nest. Path integration and view-based landmark guidance are the key strategies for the ants’ navigation. For instance, they memorise different views in a sequence (sequential memory) but also have a step counter that informs them about the covered distance during each foraging trip (odometer). The sequential memory and the odometer information can act as contextual cues during travel for retrieving the appropriate stored view. When and which cue is used at different stages and lengths of the foraging trips is still unknown. In this study, we examined how the Australian desert ant Melophorus bagoti uses sequential memory and odometric information to retrieve visual memories. Using a set-up made out of channels and two-choice boxes (Y-mazes), we demonstrate first that M. bagoti foragers are able to learn and discriminate a variety of visual stimuli in a sequence of views along the inbound trip back to the nest. We then forced the homing ants to encounter a fixed sequence of two visual patterns during their inbound trips. By manipulating the position and distance of the visual stimuli and decision boxes, we could set the two contextual cues (sequential memory and odometer) into conflict. After the short 4-m outbound distance, a preference for odometric information as a contextual cue was found, but after the long 8-m outbound distance, ants relied primarily on their sequential memory retrieval. Odometer precision deteriorates with increasing travel distance, and accordingly, our findings imply that desert ants may be relying on the most reliable contextual cue for retrieving visual memories.     

Overcoming default categorical bias in spatial memory

In the present study, we investigated whether a strong default categorical bias can be overcome in spatial memory by using alternative membership information. In three experiments, we tested location memory in a circular space while providing participants with an alternative categorization. We found that visual presentation of the boundaries of the alternative categories (Experiment 1) did not induce the use of the alternative categories in estimation. In contrast, visual cuing of the alternative category membership of a target (Experiment 2) and unique target feature information associated with each alternative category (Experiment 3) successfully led to the use of the alternative categories in estimation. Taken together, the results indicate that default categorical bias in spatial memory can be overcome when appropriate cues are provided. We discuss how these findings expand the category adjustment model (Huttenlocher, Hedges, & Duncan, 1991) in spatial memory by proposing a retrieval-based category adjustment (RCA) model.     

Interference effects by spatial proximity and age-related declines in spatial memory by Japanese monkeys (Macaca fuscata): deficits in the combined use of multiple spatial cues

Spatial information processing was assessed in 3 young (4-10 years old) and 4 aged (24-25 years old) Japanese monkeys (Macaca fuscata) on 3 delayed nonmatching-to-position (DNMP) tests with relatively short delays of 5 s. Each test had 3 conditions of different horizontal distances between sample and to-be-nonmatched positions. Experiment 1 demonstrated that the performance on the DNMP test in both age groups was impaired when 2 stimulus positions were located next to each other; however, it was fairly accurate when they were located farther apart, suggesting that interference is introduced by spatial proximity. Experiment 2 revealed age-related differences in the situation in which an additional spatial cue, depth information, was available by extending the stimulus array of the DNMP test to a 4 x 2 matrix. In this test, young monkeys performed accurately irrespective of position distance between stimuli, whereas the aged monkeys' performance remained the same as before. Experiment 3 confirmed that the recognition ability in aged monkeys was well preserved on DNMP tests with different objects. These patterns of results indicate that the ability to use information from multiple spatial cues is not accessible to the aged monkeys.