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).     

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.     

Mantled howler monkey spatial foraging decisions reflect spatial and temporal knowledge of resource distributions

An animal’s ability to find and relocate food items is directly related to its survival and reproductive success. This study evaluates how mantled howler monkeys make spatial foraging decisions in the wild. Specifically, discrete choice models and agent-based simulations are used to test whether mantled howler monkeys on Barro Colorado Island, Panama, integrate spatial information in order to maximize new leaf flush and fruit gain while minimizing distance traveled. Several heuristic models of decision making are also tested as possible alternative strategies (movement to core home range areas instead of individual trees, travel along a sensory gradient, movement along arboreal pathway networks without a predetermined destination, straight-line travel in a randomly chosen direction, and random walks). Results indicate that although leaves are the single most abundant item in the mantled howler monkey diet, long-distance travel bouts target the areas with the highest concentrations of mature fruits. Observed travel patterns yielded larger estimated quantities of fruit in shorter distances traveled than all alternative foraging strategies. Thus, this study both provides novel information regarding how primates select travel paths and suggests that a highly folivorous primate integrates knowledge of spatiotemporal resource distributions in highly efficient foraging strategies.     

Performance on the Hamilton search task,and the influence of lateralization,in captive orange-winged Amazon parrots (Amazona amazonica)

Psittacines are generally considered to possess cognitive abilities comparable to those of primates. Most psittacine research has evaluated performance on standardized complex cognition tasks, but studies of basic cognitive processes are limited. We tested orange-winged Amazon parrots (Amazona amazonica) on a spatial foraging assessment, the Hamilton search task. This task is a standardized test used in human and non-human primate studies. It has multiple phases, which require trial and error learning, learning set breaking, and spatial memory. We investigated search strategies used to complete the task, cognitive flexibility, and long-term memory for the task. We also assessed the effects of individual strength of motor lateralization (foot preference) and sex on task performance. Almost all (92 %) of the parrots acquired the task. All had significant foot preferences, with 69 % preferring their left foot, and showed side preferences contralateral to their preferred limb during location selection. The parrots were able to alter their search strategies when reward contingencies changed, demonstrating cognitive flexibility. They were also able to remember the task over a 6-month period. Lateralization had a significant influence on learning set acquisition but no effect on cognitive flexibility. There were no sex differences. To our knowledge, this is the first cognitive study using this particular species and one of the few studies of cognitive abilities in any Neotropical parrot species.     

Evidence against integration of spatial maps in humans: generality across real and virtual environments

A real-world open-field search task was implemented with humans as an analogue of Blaisdell and Cook’s (Anim Cogn 8:7–16, 2005) pigeon foraging task and Sturz, Bodily, and Katz’s (Anim Cogn 9:207–217, 2006) human virtual foraging task to 1) determine whether humans were capable of integrating independently learned spatial maps and 2) make explicit comparisons of mechanisms used by humans to navigate real and virtual environments. Participants searched for a hidden goal located in one of 16 bins arranged in a 4 × 4 grid. In Phase 1, the goal was hidden between two landmarks (blue T and red L). In Phase 2, the goal was hidden to the left and in front of a single landmark (blue T). Following training, goal-absent trials were conducted in which the red L from Phase 1 was presented alone. Bin choices during goal-absent trials assessed participants’ strategies: association (from Phase 1), generalization (from Phase 2), or integration (combination of Phase 1 and 2). Results were inconsistent with those obtained with pigeons but were consistent with those obtained with humans in a virtual environment. Specifically, during testing, participants did not integrate independently learned spatial maps but used a generalization strategy followed by a shift in search behavior away from the test landmark. These results were confirmed by a control condition in which a novel landmark was presented during testing. Results are consistent with the bulk of recent findings suggesting the use of alternative navigational strategies to cognitive mapping. Results also add to a growing body of literature suggesting that virtual environment approaches to the study of spatial learning and memory have external validity and that spatial mechanisms used by human participants in navigating virtual environments are similar to those used in navigating real-world environments.     

A socioecological perspective on primate cognition,past and present

The papers in this special issue examine the relationship between social and ecological cognition in primates. We refer to the intersection of these two domains as socioecological cognition. Examples of socioecological cognition include socially learned predator alarm calls and socially sensitive foraging decisions. In this review we consider how primate cognition may have been shaped by the interaction of social and ecological influences in their evolutionary history. The ability to remember distant, out-of-sight locations is an ancient one, shared by many mammals and widespread among primates. It seems some monkeys and apes have evolved the ability to form more complex representations of resources, integrating “what-where-how much” information. This ability allowed anthropoids to live in larger, more cohesive groups by minimizing competition for limited resources between group members. As group size increased, however, competition for resources also increased, selecting for enhanced social skills. Enhanced social skills in turn made a more sophisticated relationship to the environment possible. The interaction of social and ecological influences created a spiraling effect in the evolution of primate intelligence. In contrast, lemurs may not have evolved the ability to form complex representations which would allow them to consider the size and location of resources. This lack in lemur ecological cognition may restrict the size of frugivorous lemur social groups, thereby limiting the complexity of lemur social life. In this special issue, we have brought together two review papers, five field studies, and one laboratory study to investigate the interaction of social and ecological factors in relation to foraging. Our goal is to stimulate research that considers social and ecological factors acting together on cognitive evolution, rather than in isolation. Cross fertilization of experimental and observational studies from captivity and the field is important for increasing our understanding of this relationship. This contribution is part of the Special Issue “A Socioecological Perspective on Primate Cognition”.     

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).     

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).     

Realization,explanation and the mind-body relation

The Morris water maze has been put forward in the philosophy of neuroscience as an example of an experimental arrangement that may be used to delineate the cognitive faculty of spatial memory (e.g., Craver and Darden, Theory and method in the neurosciences, University of Pittsburgh Press, Pittsburgh, 2001; Craver, Explaining the brain: Mechanisms and the mosaic unity of neuroscience, Oxford University Press, Oxford, 2007). However, in the experimental and review literature on the water maze throughout the history of its use, we encounter numerous responses to the question of “what” phenomenon it circumscribes ranging from cognitive functions (e.g., “spatial learning”, “spatial navigation”), to representational changes (e.g., “cognitive map formation”) to terms that appear to refer exclusively to observable changes in behavior (e.g., “water maze performance”). To date philosophical analyses of the water maze have not been directed at sorting out what phenomenon the device delineates nor the sources of the different answers to the question of what. I undertake both of these tasks in this paper. I begin with an analysis of Morris’s first published research study using the water maze and demonstrate that he emerged from it with an experimental learning paradigm that at best circumscribed a discrete set of observable changes in behavior. However, it delineated neither a discrete set of representational changes nor a discrete cognitive function. I cite this in combination with a reductionist-oriented research agenda in cellular and molecular neurobiology dating back to the 1980s as two sources of the lack of consistency across the history of the experimental and review literature as to what is under study in the water maze.     

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).     

Chimpanzees and bonobos exhibit divergent spatial memory development

Spatial cognition and memory are critical cognitive skills underlying foraging behaviors for all primates. While the emergence of these skills has been the focus of much research on human children, little is known about ontogenetic patterns shaping spatial cognition in other species. Comparative developmental studies of nonhuman apes can illuminate which aspects of human spatial development are shared with other primates, versus which aspects are unique to our lineage. Here we present three studies examining spatial memory development in our closest living relatives, chimpanzees (Pan troglodytes) and bonobos (P. paniscus). We first compared memory in a naturalistic foraging task where apes had to recall the location of resources hidden in a large outdoor enclosure with a variety of landmarks (Studies 1 and 2). We then compared older apes using a matched memory choice paradigm (Study 3). We found that chimpanzees exhibited more accurate spatial memory than bonobos across contexts, supporting predictions from these species’ different feeding ecologies. Furthermore, chimpanzees – but not bonobos – showed developmental improvements in spatial memory, indicating that bonobos exhibit cognitive paedomorphism (delays in developmental timing) in their spatial abilities relative to chimpanzees. Together, these results indicate that the development of spatial memory may differ even between closely related species. Moreover, changes in the spatial domain can emerge during nonhuman ape ontogeny, much like some changes seen in human children.     

Intrinsic and extrinsic contributions to heavy tails in visual foraging

Eyes move over visual scenes to gather visual information. Studies have found heavy-tailed distributions in measures of eye movements during visual search, which raises questions about whether these distributions are pervasive to eye movements, and whether they arise from intrinsic or extrinsic factors. Three different measures of eye movement trajectories were examined during visual foraging of complex images, and all three were found to exhibit heavy tails: Spatial clustering of eye movements followed a power law distribution, saccade length distributions were lognormally distributed, and the speeds of slow, small amplitude movements occurring during fixations followed a 1/f spectral power law relation. Images were varied to test whether the spatial clustering of visual scene information is responsible for heavy tails in eye movements. Spatial clustering of eye movements and saccade length distributions were found to vary with image type and task demands, but no such effects were found for eye movement speeds during fixations. Results showed that heavy-tailed distributions are general and intrinsic to visual foraging, but some of them become aligned with visual stimuli when required by task demands. The potentially adaptive value of heavy-tailed distributions in visual foraging is discussed.     

Uniquely primate,uniquely human

Two hypotheses about primate cognition are proposed. First, it is proposed that primates, but not other mammals, understand categories of relations among external entities. In the physical domain primates have special skills in tasks such as oddity, transitivity, and relation matching that require facility with relational categories; in the social domain primates have special skills in understanding the third-party social relationships that hold among other individuals in their groups. Second, it is proposed that humans, but not other primates, understand the causal and intentional relations that hold among external entities. In the physical domain only humans understand causal forces as mediating the connection between sequentially ordered events; in the social domain only humans understand the behavior of others as intentionally directed and controlled by desired outcomes. Both these uniquely primate and these uniquely human cognitive skills are hypothesized to have their origins in adaptations for negotiating complex social interactions.     

Where am I and how will I get there from here? A role for posterior parietal cortex in the integration of spatial information and route planning

The ability of an organism to accurately navigate from one place to another requires integration of multiple spatial constructs, including the determination of one's position and direction in space relative to allocentric landmarks, movement velocity, and the perceived location of the goal of the movement. In this review, we propose that while limbic areas are important for the sense of spatial orientation, the posterior parietal cortex is responsible for relating this sense with the location of a navigational goal and in formulating a plan to attain it. Hence, the posterior parietal cortex is important for the computation of the correct trajectory or route to be followed while navigating. Prefrontal and motor areas are subsequently responsible for executing the planned movement. Using this theory, we are able to bridge the gap between the rodent and primate literatures by suggesting that the allocentric role of the rodent PPC is largely analogous to the egocentric role typically emphasized in primates, that is, the integration of spatial orientation with potential goals in the planning of goal-directed movements.     

Mirror neurons and the phenomenology of intersubjectivity

The neurological discovery of mirror neurons is of eminent importance for the phenomenological theory of intersubjectivity. G. Rizzolatti and V. Gallese found in experiments with primates that a set of neurons in the premotor cortex represents the visually registered movements of another animal. The activity of these mirror neurons presents exactly the same pattern of activity as appears in the movement of one's own body. These findings may be extended to other cognitive and emotive functions in humans. I show how these neurological findings might be “translated” phenomenologically into our own experienced sensations, feelings and volitions.     

Mental maps in chacma baboons (<Emphasis Type="Italic">Papio ursinus</Emphasis>): using inter-group encounters as a natural experiment

Encounters between groups of wild chacma baboons (Papio ursinus) can be viewed as a natural experiment to investigate the nature of these primates’ mental representations of large-scale space. During a 16-month field study in a high population density habitat we recorded the foraging routes and the most important resources of a group of 25 individuals. Also, we estimated the locations of additional baboon groups relative to the study group. Routes were less linear, travel speed was higher, and inter-resource distances were larger when other groups were present within 500 m of the focal group; thus, the study group avoided others by taking detours. We predicted that evasive manoeuvres would be characteristic of different possible orientation mechanisms, and compared them with our observations. We analysed 34 evasive manoeuvres in detail. In an area that lacked prominent landmarks, detours were small; larger detours occurred when resources were directly visible, or in the vicinity of a hill offering conspicuous landmarks. In areas without prominent landmarks, detours were along familiar routes and waiting bouts of up to 60 min occurred; on one occasion the study group aborted their entire day’s journey. We discuss these findings in the light of time and energy costs and suggest that the baboons lack the ability to compute Euclidean relations among locations, but use network maps to find their way to out-of-sight locations. This contribution is part of the Special Issue “A Socioecological Perspective on Primate Cognition” (Cunningham and Janson 2007a).     

Nomadic inhibition of attention and motor responses

Klein and MacInnes [Klein, R. M., & MacInnes, W. J. (1999). Inhibition of return is a foraging facilitator in visual search. Psychological Science, 10, 346-352] posited that the function of a phenomenon known as the inhibition of return (IOR) [Posner, M. I., & Cohen, Y. (1984). Components of visual orienting. In H. Bouma, & D. G. Bouwhuis (Eds.), Attention and performance X: Control of language processes (pp. 531-554). Hillsdale, NJ: Erlbaum] is to facilitate the foraging of food and objects in the environment. Once a target object has been identified either the location of that target in space or a movement to that target is inhibited in order to allow the performer to shift his/her attention to something new. Interestingly, in the majority of IOR studies, participants begin their search from a central home position. This research examined IOR in a nomadic target-target paradigm in which the home position randomly appeared at one of three target locations and attentional shifts/movements progressed to other locations. In Experiment 1, participants executed simple manual button presses in response to the sequential presentation of a home position and then two target stimuli. In Experiment 2, participants made manual-aiming movements in response to the same type of presentation. Results obtained from both experiments implicate perceptual-motor mechanisms over and above the inhibition of a specific target location or response. Inhibitory effects appear to be associated with both perceptual and motor processes, and depend not only on the temporal and spatial relations between potential targets, but also on the actions required to detect or engage the targets.     

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.     

The ecology of spatial memory in four lemur species

Evolutionary theories suggest that ecology is a major factor shaping cognition in primates. However, there have been few systematic tests of spatial memory abilities involving multiple primate species. Here, we examine spatial memory skills in four strepsirrhine primates that vary in level of frugivory: ruffed lemurs (Varecia sp.), ring-tailed lemurs (Lemur catta), mongoose lemurs (Eulemur mongoz), and Coquerel’s sifakas (Propithecus coquereli). We compare these species across three studies targeting different aspects of spatial memory: recall after a long-delay, learning mechanisms supporting memory and recall of multiple locations in a complex environment. We find that ruffed lemurs, the most frugivorous species, consistently showed more robust spatial memory than the other species across tasks—especially in comparison with sifakas, the most folivorous species. We discuss these results in terms of the importance of considering both ecological and social factors as complementary explanations for the evolution of primate cognitive skills.     

Consciousness,Trauma, and Health: A Cognitive Systems Response to Payne,Walsh, and Oman

Religion and cognitive science contribute complementary understandings of the human person, and an integrated perspective can bridge clinical, spiritual, and philosophical resources to facilitate healing and growth. Drawing upon cognitive science and systems theory, I respond to Richard Payne, Mary Walsh, and Doug Oman’s comments on my Mind, Brain, and the Elusive Soul (Graves 2008; Oman 2011; Payne 2011; Walsh 2011).