Spatial memory and foraging competition in captive western lowland gorillas (Gorilla gorilla gorilla)

Spatial memory and foraging competition were investigated in three mother/offspring pairs of western lowland gorillas,Gorilla gorilla gorilla, using a naturalistic foraging task at the Toronto Zoo. Sixteen permanent food sites were placed throughout the animals’ enclosures. All of the sites were baited and a pair of animals was free to visit the sites and collect the food. Five of the subjects collected the food with accuracy better than chance. Most of the subjects visited the sites using a pattern, and for half the subjects this was one of adjacency. The high accuracy of five of the subjects and the lack of a consistent adjacency pattern suggest that the animals did in fact use spatial memory. Furthermore, the gorillas tended to avoid visiting food sites that had been previously depleted by their partner. They also appeared to split their search of the enclosures, each visiting only a proportion of the food sites. This indicated that the animals were competing and altering their foraging behaviour based on the behaviour of their partner. Therefore, accuracy was recalculated to take this into account. When the sites depleted by either animal in a pair during a given trial were worked into the accuracy calculations for individual animals, three of the animals still maintained accuracy above chance. This suggests that the animals were not only able to remember which sites they had depleted, but those sites depleted by their foraging partner as well.     

Language-trained chimpanzees (Pan troglodytes) delay gratification by choosing token exchange over immediate reward consumption

Token exchange inherently introduces an element of delay between behavior and reward and so token studies may help us better understand delay of gratification and self-control. To examine this possibility, we presented three language-trained chimpanzees with repeated choices involving different foods that could be eaten immediately or lexigram (graphic symbol) tokens that represented (and could be traded for) foods later. When both options were foods, chimpanzees always chose more preferred foods over less preferred foods. When both options were lexigram tokens representing those same foods, performance remained the same as chimpanzees selected the higher value token and then traded it for food. Then, when faced with choosing a token that could be traded later or choosing a food item that could be eaten immediately, most chimpanzees learned to make whatever response led to the more preferred food. They did this even when that meant selecting a high value lexigram token that could be traded only 2 to 3 min later instead of a medium value, but immediately available, food item. Thus, chimpanzees flexibly selected tokens even though such selections necessarily delayed gratification and required forgoing immediately available food. This finding illustrates the utility of symbolic token exchange for assessing self-control in nonhuman animals.     

Uncertain availability of a preferred food affects choice in a captive group of chimpanzees (Pan troglodytes)

Food-choice was investigated in a social group of 16 chimpanzees (Pan troglodytes) maintained in a large outdoor compound. Three feeding stations located along the periphery of the compound were considered analogous to food patches. Color-coded aluminum panels temporarily covered each feeding apparatus, with one color corresponding to nonpreferred food (commercial biscuits) available at two locations and other colors corresponding to the certain or uncertain availability of preferred food (oranges) available at one location. Only nine chimpanzees met the criterion for learning the color/food associations and thus only those animals were included in the analysis. There was a significant decrease in choosing the station associated with oranges when the probability of availability of oranges was reduced from 0.5 to 0.1 but not from 1.0 to 0.5. In addition, there was a significant increase in the frequency with which the subjects made no choice when the probability of availability of oranges was reduced from 1.0 to 0.1. The data indicate that the uncertain availability of preferred food in a choice situation affects choice behavior in a social group of chimpanzees studied under controlled conditions.     

Some characteristics of spatial associative memory in the pigeon, Columba livia

Willson and Wilkie (1993) developed a novel procedure to assess pigeons' memory for the spatial location of food. Only one of four locations provided food each daily session. Each location consisted of an illuminated pecking key and grain feeder. Over different days different locations, randomly selected, provided food during a 16-min session. The pigeons tended to revisit the location at which food was found on the previous day thereby demonstrating memory for food-spatial location associations over 24 h. Three experiments were conducted to further investigate this phenomenon. In Experiment 1 the session duration was varied between 4 and 32 min. Longer sessions had no detectable effect on their ability to remember the rewarded location 24 h later, a result that suggests that only brief encounters with food at a particular location are necessary for recall. In Experiment 2 the necessity of an active search for the day's rewarded location was removed; a 5-min period in which only the rewarded key was lit preceded the regular 16-min session. Pecks to the lit key in this 5-min period produced grain on the standard schedule. This manipulation facilitated the pigeons' discovery of food but did not affect their ability to remember the rewarded location, suggesting that the process of search and discovery is not essential to the associative memory process. In Experiment 3, food was available during the complete session (non-depleting condition) or was available only during the first half of the session (depleting condition). No detectable differences in the birds' memory of yesterday's profitable location were found. This suggests that non-depletion of food is not a necessary condition for day-to-day recall of food location. Taken together these findings enlarge our understanding of the spatial associative memory process.     

Episodic-like memory in the rat

A fundamental question in comparative cognition is whether animals remember unique, personal past experiences. It has long been argued that memories for specific events (referred to as episodic memory) are unique to humans. Recently, considerable evidence has accumulated to show that food-storing birds possess critical behavioral elements of episodic memory, referred to as episodic-like memory in acknowledgment of the fact that behavioral criteria do not assess subjective experiences. Here we show that rats have a detailed representation of remembered events and meet behavioral criteria for episodic-like memory. We provided rats with access to locations baited with distinctive (e.g., grape and raspberry) or nondistinctive (regular chow) flavors. Locations with a distinctive flavor replenished after a long but not a short delay, and locations with the nondistinctive flavor never replenished. One distinctive flavor was devalued after encoding its location by prefeeding that flavor (satiation) or by pairing it with lithium chloride (acquired taste aversion), while the other distinctive flavor was not devalued. The rats selectively decreased revisits to the devalued distinctive flavor but not to the nondevalued distinctive flavor. The present studies demonstrate that rats selectively encode the content of episodic-like memories.     

Elements of episodic-like memory in animals

A number of psychologists have suggested that episodic memory is a uniquely human phenomenon and, until recently, there was little evidence that animals could recall a unique past experience and respond appropriately. Experiments on food-caching memory in scrub jays question this assumption. On the basis of a single caching episode, scrub jays can remember when and where they cached a variety of foods that differ in the rate at which they degrade, in a way that is inexplicable by relative familiarity. They can update their memory of the contents of a cache depending on whether or not they have emptied the cache site, and can also remember where another bird has hidden caches, suggesting that they encode rich representations of the caching event. They make temporal generalizations about when perishable items should degrade and also remember the relative time since caching when the same food is cached in distinct sites at different times. These results show that jays form integrated memories for the location, content and time of caching. This memory capability fulfils Tulving's behavioural criteria for episodic memory and is thus termed 'episodic-like'. We suggest that several features of episodic memory may not be unique to humans.     

Do chimpanzees know what conspecifics know?

We conducted three experiments on social problem solving by chimpanzees, Pan troglodytes. In each experiment a subordinate and a dominant individual competed for food, which was placed in various ways on the subordinate's side of two opaque barriers. In some conditions dominants had not seen the food hidden, or food they had seen hidden was moved elsewhere when they were not watching (whereas in control conditions they saw the food being hidden or moved). At the same time, subordinates always saw the entire baiting procedure and could monitor the visual access of their dominant competitor as well. If subordinates were sensitive to what dominants did or did not see during baiting, they should have preferentially approached and retrieved the food that dominants had not seen hidden or moved. This is what they did in experiment 1 when dominants were either uninformed or misinformed about the food's location. In experiment 2 subordinates recognized, and adjusted their behaviour accordingly, when the dominant individual who witnessed the hiding was replaced with another dominant individual who had not witnessed it, thus demonstrating their ability to keep track of precisely who has witnessed what. In experiment 3 subordinates did not choose consistently between two pieces of hidden food, one of which dominants had seen hidden and one of which they had not seen hidden. However, their failure in this experiment was likely to be due to the changed nature of the competition under these circumstances and not to a failure of social-cognitive skills. These findings suggest that at least in some situations (i.e. competition with conspecifics) chimpanzees know what conspecifics have and have not seen (do and do not know), and that they use this information to devise effective social-cognitive strategies. Copyright 2001 The Association for the Study of Animal Behaviour.     

Elements of episodic-like memory in animal models

Representations of unique events from one’s past constitute the content of episodic memories. A number of studies with non-human animals have revealed that animals remember specific episodes from their past (referred to as episodic-like memory). The development of animal models of memory holds enormous potential for gaining insight into the biological bases of human memory. Specifically, given the extensive knowledge of the rodent brain, the development of rodent models of episodic memory would open new opportunities to explore the neuroanatomical, neurochemical, neurophysiological, and molecular mechanisms of memory. Development of such animal models holds enormous potential for studying functional changes in episodic memory in animal models of Alzheimer’s disease, amnesia, and other human memory pathologies. This article reviews several approaches that have been used to assess episodic-like memory in animals. The approaches reviewed include the discrimination of what, where, and when in a radial arm maze, dissociation of recollection and familiarity, object recognition, binding, unexpected questions, and anticipation of a reproductive state. The diversity of approaches may promote the development of converging lines of evidence on the difficult problem of assessing episodic-like memory in animals.     

A fruit in the hand or two in the bush? Divergent risk preferences in chimpanzees and bonobos

Human and non-human animals tend to avoid risky prospects. If such patterns of economic choice are adaptive, risk preferences should reflect the typical decision-making environments faced by organisms. However, this approach has not been widely used to examine the risk sensitivity in closely related species with different ecologies. Here, we experimentally examined risk-sensitive behaviour in chimpanzees (Pan troglodytes) and bonobos (Pan paniscus), closely related species whose distinct ecologies are thought to be the major selective force shaping their unique behavioural repertoires. Because chimpanzees exploit riskier food sources in the wild, we predicted that they would exhibit greater tolerance for risk in choices about food. Results confirmed this prediction: chimpanzees significantly preferred the risky option, whereas bonobos preferred the fixed option. These results provide a relatively rare example of risk-prone behaviour in the context of gains and show how ecological pressures can sculpt economic decision making.     

Chimpanzee nest distribution and site reuse in a dry habitat: implications for early hominin ranging

This paper reports on a 20-month study of chimpanzee nesting patterns in Issa, Ugalla, western Tanzania. Ugalla is one of the driest, most open, and seasonal habitats where chimpanzees are found. The methods used were ethoarchaeological, as the chimpanzees were not habituated and behavioural observations were rare. Systematic data on the spatial and temporal distribution of nests are presented. Places with no nests at the beginning of the study, despite being suitable for nesting, were used as controls. Similar to other chimpanzee study sites, nests were highly concentrated in some parts of the landscape. Issa chimpanzees preferred to nest on slopes. They extensively used the woodland vegetation type of their habitat for nesting throughout the annual cycle. Ninety percent of nest sites were used repeatedly throughout the study period, but none of the control places had nests during this period. The results indicate that chimpanzees ranged more widely during the dry season, when food abundance was lowest, food was available mainly in open vegetation types, and when drinking water was restricted to a few sources. Early hominins in similar habitats may have followed the ranging strategy of Issa chimpanzees. As with a previous study, the distribution of nests was spatially similar to archaeological distributions in early hominin sites. Hominin topography and vegetation type preferences may be misrepresented in the archaeological record. Nest sites may have been the antecedents of carcass processing sites.     

Development of the visual preference of chimpanzees (<Emphasis Type="Italic">Pan troglodytes</Emphasis>) for photographs of primates: effect of social experience

In a study by Tanaka (2003) five captive chimpanzees preferred photographs of humans to those of chimpanzees. All the subjects were raised by humans and lived in captivity for many years. This suggests their preference might have developed through social experience. In this study examined this hypothesis by using three young chimpanzees raised by their mothers in a captive chimpanzee community. The young chimpanzees were tested four times before six years of age. I also tested eight adult chimpanzees that had been in captivity for more than 20 years. Each subject was presented with digitized color photographs of different species of primates on a touch-sensitive screen. The subjects received a food reward when they touched a photograph, irrespective of which photograph they touched. All the adult chimpanzees touched photographs of humans more frequently than those of any other species of primate. Two of the young chimpanzees showed no species preference before reaching 5 years of age, when they started to show preference for humans. The remaining young chimpanzee consistently preferred chimpanzees. These results suggest that development of visual preference of chimpanzees is affected by social experience during infancy.     

Mental map in wild chimpanzees: An analysis of hammer transports for nut cracking

The mental map of wild chimpanzees is analyzed in the context of their transports of clubs and stones used for cracking two species of nuts of different hardness,Coula edulis andPanda oleosa, in the Tai National Park (Ivory Coast). For the harderPanda nuts, they transport the harder hammers, i.e., almost exclusively stones, hammers of greater weight, and the transports are longer than forCoula nuts. The analysis made for the transports forPanda nuts shows that they seem to remember the location of stones and to choose the stones so as to keep the transport distance minimal. The chimpanzees seem to possess an Euclidian space, which allows them to somehow measure and remember distances; to compare several such distances so as to choose the stone with the shortest distance to a goal tree; to correctly locate a new stone location with reference to different trees; and to change their reference point so as to measure the distance to eachPanda tree from any stone location. They also combine the weight and the distance. The wild chimpanzees of the Tai National Park seem to possess concrete operation abilities in spatial representation.     

Can Black‐and‐White Ruffed Lemurs (Varecia variegata) Solve Object Permanence Tasks?

We examined object permanence in black‐and‐white‐ruffed lemurs (Varecia variegata) at Zoo Atlanta. A series of visible and invisible displacement tasks with suitable controls were presented to five adult subjects. Subjects performed significantly above chance on all regular tasks, except for the double invisible displacements. Subjects failed visible and invisible controls. Failure on the control trials did not appear to be because subjects used the “last box touched” strategy (subjects did not choose the last box touched significantly more than expected by chance). However, a substantial percentage of choices was made to the last box touched by the experimenter. There was no significant difference between this percentage, and the percentage of choices made to the baited box (on both visible and invisible controls), which indicates that subjects were drawn to both boxes which the experimenter visited/touched, and thus failed the controls. Based on the results from the present study, we believe that there is no evidence that black‐and‐white ruffed lemurs understand visible and invisible tasks in the traditional object permanence battery. Am. J. Primatol. 75:376‐386, 2013. © 2013 Wiley Periodicals, Inc.     

Chimpanzees and bonobos distinguish between risk and ambiguity

Although recent research has investigated animal decision-making under risk, little is known about how animals choose under conditions of ambiguity when they lack information about the available alternatives. Many models of choice behaviour assume that ambiguity does not impact decision-makers, but studies of humans suggest that people tend to be more averse to choosing ambiguous options than risky options with known probabilities. To illuminate the evolutionary roots of human economic behaviour, we examined whether our closest living relatives, chimpanzees (Pan troglodytes) and bonobos (Pan paniscus), share this bias against ambiguity. Apes chose between a certain option that reliably provided an intermediately preferred food type, and a variable option that could vary in the probability that it provided a highly preferred food type. To examine the impact of ambiguity on ape decision-making, we interspersed trials in which chimpanzees and bonobos had no knowledge about the probabilities. Both species avoided the ambiguous option compared with their choices for a risky option, indicating that ambiguity aversion is shared by humans, bonobos and chimpanzees.     

Social tactics of pigs in a competitive foraging task: the 'informed forager' paradigm

Studies of the social dynamics in foraging groups have focused primarily on birds, rodents and nonhuman primates. We extended the study of animal social tactics to the domestic pig, Sus scrofa, by using an experimental analogue of natural foraging skills, the 'informed forager' paradigm. We investigated the behaviour of 16 pigs foraging in pairs in an arena in which food had been hidden in one of eight monopolizable buckets. Before each pair trial, one of the pigs, the 'informed' pig, was given privileged knowledge about the location of the food during a solitary search trial. The 'noninformed' pig was na?ve about the location of the food during pair trials, but heavier than its informed partner and thus able to displace the latter from the baited bucket. By first focusing on the informed pigs' behaviour, we show that pigs are able to remember and relocate the food site. They found the food in relocation trials, using fewer bucket investigations than expected of a random searcher. Second, by focusing on the noninformed pigs, we show that pigs are able to exploit the knowledge of others by following them to a food source. They investigated more buckets immediately after their informed partners significantly more often than expected by chance and required fewer bucket investigations to find the food in pair trials than expected from a random searcher, but not in solitary search trials. We discuss these latter findings with reference to social foraging tactics. Copyright 2000 The Association for the Study of Animal Behaviour.     

Do Children Eat What They Say? Validity of Intended Food Choices Among Native American School Children

Objective. To examine the agreement between school children's intended food choices and observed food choices. Design. Native American students in the second through fifth grade completed a questionnaire that asked them to select from 10 paired food choices for a given meal or snack. Three weeks later students chose among foods identical to those on the questionnaire as part of their usual school lunch or breakfast over three consecutive days; afternoon snacks were also offered. Results. Agreement between students' intended food choices and observed food choices was examined across 10 food pairs. The composite K coefficient between intended and observed food choices was 0.09 (95% confidence interval 0.06, 0.12), indicating virtually no agreement above that expected by chance. There were no differences in agreement by sex or grade. Conclusions. Intended food choices were not significantly associated with observed food choices. It is unclear whether intended food choices reflect nutrition knowledge, socially desirable responses, food preferences, or some other dimension of eating behavior. Although responsive to school-based nutrition interventions, the interpretation of changes in intended food choices must be clarified in future research.     

Food Preferences Among Captive Western Gorillas (Gorilla gorilla gorilla) and Chimpanzees (Pan troglodytes)

I used a zoological park setting to address food preferences among gorillas (Gorilla gorilla gorill) and chimpanzees (Pan troglodytes). Gorillas and chimpanzees are different sizes, and consequently, have been traditionally viewed as ecologically distinct. Sympatric western gorillas and chimpanzees have proved difficult to study in the wild. Limited field data have provided conflicting information about whether gorillas are fundamentally different from chimpanzees in diet and behavior. Fruit eating shapes the behavior of most apes, but it is unclear whether the large-bodied gorillas are an exception to this rule, specifically whether they are less selective and more opportunistic fruit eaters than chimpanzees are. My research provides experimental observational data to complement field data and to better characterize the diets and food preferences of the African apes. During laboratory research at the San Francisco Zoological Gardens, I examined individual and specific differences in food preferences of captive gorillas and chimpanzees via experimental paired-choice food trials with foods that varied in nutritional content. During the study, I offered 2500 paired-food choices to 6 individual gorillas and 2000 additional pairs to them as a group. I also proffered 600 food pairs to 4 individual chimpanzees. Despite expectations of the implications of body size differences for diet, gorillas and chimpanzees exhibited similar food preferences. Both species preferred foods high in non-starch sugars and sugar-to-fiber ratios, and low in total dietary fiber. Neither species avoided foods containing tannins. These data support other suggestions of African apes sharing a frugivorous adaptation.     

Sumatran Orangutans and a Yellow-Cheeked Crested Gibbon Know What Is Where

In their natural habitats orangutans and gibbons have to solve spatial problems to find enough food, which is distributed over large areas and available at different times of the year. Therefore both species should evolve spatial memory skills to remember spatial locations and their content. We conducted 2 studies in a 1900-m² naturalistic outdoor enclosure. In the 1st study, we hid kiwi pieces in 10 different locations and placed kiwi pieces in a visible location. Individuals of both species approached significantly more food locations in the test condition than in the control condition in which no food was hidden. In the 2nd study, we hid 2 types of food in 10 different locations so that individuals had to remember which food type was where. We hid bananas on trees (banana condition) and grapes under bamboo shrubs (grape condition). We also placed oranges in full view (control condition) to rule out the possibility that finding food may automatically trigger an indiscriminate search. Individuals approached the banana locations more often in the banana than in the other 2 conditions. Some orangutans, but not the gibbon, also approached the grape locations more often in the grape than in the other 2 conditions. Individuals often returned to locations in which they previously found food and rarely revisited locations in the same session. We detected little influence of the food quantity and no influence of the distance to each location on the subjects' foraging behavior.     

What,where and when: deconstructing memory

The ability of animals to remember the what, where and when of a unique past event is used as an animal equivalent to human episodic memory. We currently view episodic memory as reconstructive, with an event being remembered in the context in which it took place. Importantly, this means that the components of a what, where, when memory task should be dissociable (e.g. what would be remembered to a different degree than when). We tested this hypothesis by training hummingbirds to a memory task, where the location of a reward was specified according to colour (what), location (where), and order and time of day (when). Although hummingbirds remembered these three pieces of information together more often than expected, there was a hierarchy as to how they were remembered. When seemed to be the hardest to remember, while errors relating to what were more easily corrected. Furthermore, when appears to have been encoded as a combination of time of day and sequence information. As hummingbirds solved this task using reconstruction of different memory components (what, where and when), we suggest that similar deconstructive approaches may offer a useful way to compare episodic and episodic-like memories.     

Flexibility and persistence of chimpanzee (Pan troglodytes) foraging behavior in a captive environment

As a result of environmental variability, animals may be confronted with uncertainty surrounding the presence of, or accessibility to, food resources at a given location or time. While individuals can rely on personal experience to manage this variability, the behavior of members of an individual's social group can also provide information regarding the availability or location of a food resource. The purpose of the present study was to measure how captive chimpanzees individually and collectively adjust their foraging strategies at an artificial termite mound, as the availability of resources provided by the mound varied over a number of weeks. As predicted, fishing activity at the mound was related to resource availability. However, chimpanzees continued to fish at unbaited locations on the days and weeks after a location had last contained food. Consistent with previous studies, our findings show that chimpanzees do not completely abandon previously learned habits despite learning individually and/or socially that the habit is no longer effective.