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.     

Delay of gratification by chimpanzees (Pan troglodytes) in working and waiting situations

We tested four chimpanzees in a self-control task in which food rewards accumulated as long as they were not eaten. In one condition, the chimpanzees had to perform a computer task that directly led to the delivery of the food rewards. In another condition, working on the computerized task was not required and any such work was not linked to the delivery of rewards. The third condition offered no computerized task (chimpanzees simply waited for food rewards to be delivered). Three of four chimpanzees showed no effect of the work scenario on delay of gratification. The one chimpanzee that showed an influence of work scenario on self-control was the overall poorest performing animal. This animal delayed gratification the longest, however, when work was required and reward delivery was directly linked to that work. Therefore, although there is little evidence linking delay of gratification to work requirements in chimpanzees, chimpanzees with lower overall self-control might benefit from having some work available if reward accumulation is contingent on performing that work.     

Dogs (Canis familiaris), but not chimpanzees (Pan troglodytes), understand imperative pointing

Chimpanzees routinely follow the gaze of humans to outside targets. However, in most studies using object choice they fail to use communicative gestures (e.g. pointing) to find hidden food. Chimpanzees' failure to do this may be due to several difficulties with this paradigm. They may, for example, misinterpret the gesture as referring to the opaque cup instead of the hidden food. Or perhaps they do not understand informative communicative intentions. In contrast, dogs seem to be skilful in using human communicative cues in the context of finding food, but as of yet there is not much data showing whether they also use pointing in the context of finding non-food objects. Here we directly compare chimpanzees' (N = 20) and dogs' (N = 32) skills in using a communicative gesture directed at a visible object out of reach of the human but within reach of the subject. Pairs of objects were placed in view of and behind the subjects. The task was to retrieve the object the experimenter wanted. To indicate which one she desired, the experimenter pointed imperatively to it and directly rewarded the subject for handing over the correct one. While dogs performed well on this task, chimpanzees failed to identify the referent. Implications for great apes' and dogs' understanding of human communicative intentions are discussed.     

Differential use of attentional and visual communicative signaling by orangutans (Pongo pygmaeus) and gorillas (Gorilla gorilla) in response to the attentional status of a human

In this study we investigated the communicative abilities of 10 orangutans (Pongo pygmaeus) and seven western lowland gorillas (Gorilla gorilla gorilla), and particularly focused on their sensitivity to the attentional state of a human experimenter when choosing from a repertoire of both auditory and visual communication strategies. In experiment 1 a banana was placed in front of the subject's cage and a human experimenter was either present or absent. The subject's behavior was recorded for 60 sec. Both gorillas and orangutans gestured (t(16)=-3.58, P<.005) and vocalized (t(16)=-2.47, P<.05) more when the experimenter was present. In experiment 2 a human experimenter held a banana in front of the subject's cage and was oriented either toward or away from the subject. Again the subject's behavior was recorded for 60 sec. In this experiment both gorillas and orangutans gestured significantly more frequently (t(16)=3.40, P<.005) when the experimenter was oriented toward them. In addition, gorillas and orangutans used other forms of visual communication signals, such as lip pout (t(16)=3.66, P<.005), barter/trade (t(16)=2.31, P<.05), and body present (t(16)=2.31, P<.05) significantly more when an experimenter was facing them. The overall results indicate that both gorillas and orangutans are sensitive to the attentional state of a human experimenter and use appropriate communicative signals to gain that individual's attention. These results are also similar to previous findings on communicative behaviors in chimpanzees.     

Food-exchange with humans in brown capuchin monkeys

To assess how brown capuchin monkeys (Cebus apella) delay gratification and maximize payoff, we carried out four experiments in which six subjects could exchange food pieces with a human experimenter. The pieces differed either in quality or quantity. In qualitative exchanges, all subjects gave a piece of food to receive another of higher value. When the difference of value between the rewards to be returned and those expected was higher, subjects performed better. Only two subjects refrained from nibbling the piece of food before returning it. All subjects performed two or three qualitative exchanges in succession to obtain a given reward. In quantitative exchanges, three subjects returned a food item to obtain a bigger one, but two of them nibbled the item before returning it. Individual differences were marked. Subjects had some difficulties when the food to be returned was similar or equal in quality to that expected.     

Tactical use of unimodal and bimodal communication by chimpanzees, Pan troglodytes

Do chimpanzees tailor their communication in accordance with the attentional status of a human observer? We presented 57 chimpanzees with three experimental conditions in randomized order: an experimenter offered a banana to the focal subject (Focal), to a cagemate of the focal subject (In-Cage) and to a chimpanzee in an adjacent cage (Adjacent) while a second experimenter recorded the first and second responses of the focal subject in all three conditions. The chimpanzees' behaviour was mostly visual or bimodal in the Focal condition, changing to auditory behaviour or disengagement in the In-Cage and Adjacent conditions. Thus, with no explicit training and on their first trials in all instances, the chimpanzees tactically deployed their communicative behaviours in the visual and auditory domains in accordance with the manipulated attentional and intentional status of a human observer.     

Assessing burrowing, nest construction, and hoarding in mice

Deterioration in the ability to perform "Activities of daily living" (ADL) is an early sign of Alzheimer's disease (AD). Preclinical behavioural screening of possible treatments for AD currently largely focuses on cognitive testing, which frequently demands expensive equipment and lots of experimenter time. However, human episodic memory (the most severely affected aspect of memory in AD) is different to rodent memory, which seems to be largely non-episodic. Therefore the present ways of screening for new AD treatments for AD in rodents are intrinsically unlikely to succeed. A new approach to preclinical screening would be to characterise the ADL of mice. Fortuitously, several such assays have recently been developed at Oxford, and here the three most sensitive and well-characterised are presented. Burrowing was first developed in Oxford. It evolved from a need to develop a mouse hoarding paradigm. Most published rodent hoarding paradigms required a distant food source to be linked to the home cage by a connecting passage. This would involve modifying the home cage as well as making a mouse-proof connecting passage and food source. So it was considered whether it would be possible to put the food source inside the cage. It was found that if a container was placed on the floor it was emptied by the next morning., The food pellets were, however, simply deposited in a heap at the container entrance, rather than placed in a discrete place away from the container, as might be expected if the mice were truly hoarding them. Close inspection showed that the mice were performing digging ("burrowing") movements, not carrying the pellets in their mouths to a selected place as they would if truly hoarding them. Food pellets are not an essential substrate for burrowing; mice will empty tubes filled with sand, gravel, even soiled bedding from their own cage. Moreover, they will empty a full tube even if an empty one is placed next to it. Several nesting protocols exist in the literature. The present Oxford one simplifies the procedure and has a well-defined scoring system for nest quality. A hoarding paradigm was later developed in which the mice, rather than hoarding back to the real home cage, were adapted to living in the "home base" of a hoarding apparatus. This home base was connected to a tube made of wire mesh, the distal end of which contained the food source. This arrangement proved to yield good hoarding behaviour, as long as the mice were adapted to living in the "home base" during the day and only allowed to enter the hoarding tube at night.     

Tradeoffs among delay, rate, and amount of reinforcement

In Experiment 1, an adjusting-delay procedure was used to measure pigeons' choices between a single delayed reinforcer and a range of different variable-time schedules. Indifference points showed an inverse relation between rate of reinforcement and delay that was well described by a hyperbolic equation. An adjusting-amount procedure was used in Experiment 2, in which pigeons chose between an adjusting amount of food delivered after a 0.5-s delay and 3 s of food delivered after a range of different delays, and the effects of delay were similar to those found in Experiment 1. The results from both experiments indicated that, for pigeons, the strength of a reinforcer decreased rapidly with increasing delay. Estimates of a decay rate parameter in the hyperbolic equation were similar to those found in other studies with pigeons, but the rates of temporal discounting were three or four times faster than those found in studies with rats, suggesting a possible species difference.     

Are apes really inequity averse?

Brosnan et al. (Brosnan, S. F. Schiff, H. C. & de Waal, F. B. M. 2005 Tolerance for inequity may increase with social closeness in chimpanzees. Proc. R. Soc. B272, 253-258) found that chimpanzees showed increased levels of rejection for less-preferred food when competitors received better food than themselves and postulated as an explanation inequity aversion. In the present study, we extended these findings by adding important control conditions, and we investigated whether inequity aversion could also be found in the other great ape species and whether it would be influenced by subjects' relationship with the competitor. In the present study, subjects showed a pattern of food rejection opposite to the subjects of the above study by Brosnan et al. (2005). Our apes ignored fewer food pieces and stayed longer in front of the experimenter when a conspecific received better food than themselves. Moreover, chimpanzees begged more vigorously when the conspecific got favoured food. The most plausible explanation for these results is the food expectation hypothesis - seeing another individual receive high-quality food creates the expectation of receiving the same food oneself - and not inequity aversion.     

The Relationship between Event-Based Prospective Memory and Ongoing Task Performance in Chimpanzees (Pan troglodytes)

Prospective memory is remembering to do something at a future time. A growing body of research supports that prospective memory may exist in nonhuman animals, but the methods used to test nonhuman prospective memory differ from those used with humans. The current work tests prospective memory in chimpanzees using a method that closely approximates a typical human paradigm. In these experiments, the prospective memory cue was embedded within an ongoing task. Tokens representing food items could be used in one of two ways: in a matching task with pictures of items (the ongoing task) or to request a food item hidden in a different location at the beginning of the trial. Chimpanzees had to disengage from the ongoing task in order to use the appropriate token to obtain a higher preference food item. In Experiment 1, chimpanzees effectively matched tokens to pictures, when appropriate, and disengaged from the ongoing task when the token matched the hidden item. In Experiment 2, performance did not differ when the target item was either hidden or visible. This suggested no effect of cognitive load on either the prospective memory task or the ongoing task, but performance was near ceiling, which may have contributed to this outcome. In Experiment 3, we created a more challenging version of the task. More errors on the matching task occurred before the prospective memory had been carried out, and this difference seemed to be limited to the hidden condition. This finding parallels results from human studies and suggests that working memory load and prospective memory may have a similar relationship in nonhuman primates.     

Delay Maintenance in Tonkean Macaques (<Emphasis Type="BoldItalic">Macaca tonkeana</Emphasis>) and Brown Capuchin Monkeys (<Emphasis Type="BoldItalic">Cebus apella</Emphasis>)

Animals commonly face choices requiring them to wait and postpone action. The ability to delay gratification is a prerequisite for making future-oriented decisions. We investigated the ability of brown capuchins (Cebus apella) and Tonkean macaques (Macaca tonkeana) to delay benefits in several experiments. In exchange tasks, subjects had to return a piece of cookie after a given time lag to obtain a larger one from an experimenter. Capuchins could wait 10–40 s and macaques 20–80 s depending on subjects and the size of rewards. Both groups were able to anticipate delay durations, but unlike macaques, capuchins discounted all sizes of reward at the same speed, meaning that their delay-maintenance was not affected by the reward size. When the subjects could give the initial piece of cookie back immediately and then wait for the return, performances increased to 10–21 min for capuchins and 21–42 min for macaques, demonstrating the role of consumption inhibition in postponing gratification. In a further task, we presented subjects with an accumulation of food pieces added at short intervals until they seized them. On average, brown capuchins could wait 33–42 s and macaques 38–72 s before seizing the rewards. Our results confirmed that brown capuchins were more impulsive than Tonkean macaques in several tasks. We did not find significant differences between the waiting performances of the Tonkean macaques and those previously reported in long-tailed macaques. The contrasting performances of macaques and capuchins might be related to their different skills in the physical and social domains.     

Modifying the object-choice task: Is the way you look important for ravens?

Most animals seem to have difficulties in using gaze cues to find hidden food in object-choice tasks. For instance, chimpanzees usually fail in these tests, even though they are capable of following other's gaze geometrically behind barriers. Similar to chimpanzees, common ravens are skilled in tracking other's gaze but fail in object-choice tasks. We here explored whether procedural modifications, which had been used successfully in chimpanzees, would also yield positive results in ravens. In our modifications (a) the experimenter approached the cup while gazing at it, (b) the gaze cue was accompanied by a sound and (c) the experimenter could actually see the food while giving the gaze cue. Two out of seven birds performed above chance level in some of these conditions. However, we ascribe this improvement to the individuals' learning ability rather than to an understanding of the communicative nature of the task. This interpretation is further supported by results of a follow-up experiment suggesting that ravens may not rely on conspecifics' gaze cues for finding food caches in a natural foraging context. In sum, our results suggest that ravens may not transfer their gaze follow abilities to foraging situations involving hidden food.     

Ability to delay gratification and BMI in preadolescence

Delay of gratification tasks require an individual to forgo an immediate reward and wait for a more desirable delayed reward. This study used an ecologically valid measure of delayed gratification to test the hypothesis that preadolescents with higher BMI would be less likely to delay gratification. Healthy Hawks is a 12-week educational/behavioral obesity intervention at the University of Kansas Medical Center. Each week, children earn a point if they complete their goals worksheet. They can spend that point immediately on a small toy prize or save points to use on a larger prize. We retrospectively calculated the percentage of points saved over the 12 weeks for 59 children (28 females) ages 8-12 years old (mean = 10.29 ± 1.39). Spearman correlation revealed that higher BMI percentile was associated with reduced point savings (r = 0.33, P = 0.01). Similarly, obese preadolescents saved significantly fewer points than healthy weight (HW) and overweight preadolescents (t (57) = 3.14, P < 0.01). Results from our ecologically valid measure support the theory that obese children are less likely to delay gratification than overweight and HW children. Even for nonfood rewards, preadolescent children with higher BMIs prefer the immediate reward over a delayed, larger reward. This has implications for developing specific strategies within obesity treatments aimed at improving delayed gratification.     

Diet composition of chimpanzees inhabiting the montane forest of Kahuzi,Democratic Republic of Congo

The diet of chimpanzees was investigated by direct observations, feeding remains, and fecal analysis from January 1994 to December 2000 in the montane forest of Kahuzi-Biega National Park. A total of 171 food items were identified, among which 156 items were plant materials belonging to 114 species from 57 taxonomic families. Chimpanzees consumed 66 species of fruits (62 species of pulps and four species of seeds). Results of fecal analysis showed that fig fruits were the most frequently eaten. Their seeds occurred in 92% of a total of 7212 chimpanzee fecal samples. The chimpanzees changed their diet according to seasonal and annual variations in both abundance and diversity of fruit species. However, they are very selective frugivores. Only a few pulp-fruit species are regularly identified in their fecal samples. During the rainy season, when ripe fruit was scarce, chimpanzees relied heavily on piths and leaves. They swallowed leaves of two species of Commelinaceae without chewing, probably for medical purposes. Animal foods were eaten infrequently. The montane forest of Kahuzi, where chimpanzees range up to 2600 m above sea level, may be the highest altitudinal limit ever recorded for their distribution. Compared to other chimpanzee habitats, Kahuzi has a low diversity of fruit species and the availability of a few pulp-fruit species may be critical to the survival of Kahuzi chimpanzees.     

The effects of hippocampal lesions in homing pigeons on a one-trial food association task

The role of the avian hippocampal formation in a one-trial food association task was investigated across various retention intervals. Control pigeons, lesioned controls, and pigeons with hippocampal formation lesions were allowed to find food hidden in one of four uniquely decorated bowls in a specific location in a room. After retention intervals of 10 min, 1 h, 7 h, and 24 h, pigeons were placed back in the room with the same bowl in the same location (unmanipulated trials) or with the previously rewarding bowl in a new location and a different bowl in the previously rewarding location (test trials). Although all groups chose the correct bowl during unmanipulated trials, hippocampal formation lesioned birds' choices to the bowl in the correct location decreased compared to the combined controls during the test trials. The results suggest that hippocampal formation lesions do not impair long-term memory of a goal after one experience but significantly decrease the use of spatial information to return to that goal. Accepted: 18 September 1999     

Context-dependent tool use in New Caledonian crows

Humans and chimpanzees both exhibit context-dependent tool use. That is, both species choose to use tools when food is within reach, but the context is potentially hazardous. Here, we show that New Caledonian crows used tools more frequently when food was positioned next to a novel model snake than when food was positioned next to a novel teddy bear or a familiar food bowl. However, the crows showed no significant difference in their neophobic reactions towards the teddy bear and the model snake. Therefore, the crows used tools more in response to a risky object resembling a natural predator than to a less-threatening object that provoked a comparable level of neophobia. These results show that New Caledonian crows, like humans and chimpanzees, are capable of context-dependent tool use.     

The survival and transfer of microbial contamination via cloths, hands and utensils

Survival and transfer of bacteria from laminated surfaces and cleaning cloths were investigated under laboratory conditions. Drying produced substantial reductions in numbers of recoverable organisms and achieved satisfactory decontamination of clean laminate surfaces. On soiled surfaces and on clean and soiled cloths, Gram-positive and some Gram-negative species survived for up to 4 h, and in some cases up to 24 h. Where contaminated surfaces or cloths came into contact with the fingers, a stainless steel bowl, or a clean laminate surface, organisms were transferred in sufficient numbers to represent a potential hazard if in contact with food.     

The survival and transfer of microbial contamination via cloths, hands and utensils

Survival and transfer of bacteria from laminated surfaces and cleaning cloths were investigated under laboratory conditions. Drying produced substantial reductions in numbers of recoverable organisms and achieved satisfactory decontamination of clean laminate surfaces. On soiled surfaces and on clean and soiled cloths, Gram-positive and some Gram-negative species survived for up to 4 h, and in some cases up to 24 h. Where contaminated surfaces or cloths came into contact with the fingers, a stainless steel bowl, or a clean laminate surface, organisms were transferred in sufficient numbers to represent a potential hazard if in contact with food.     

Chimpanzees (Pan troglodytes) fail a what-where-when task but find rewards by using a location-based association strategy

Recollecting the what-where-when of an episode, or episodic-like memory, has been established in corvids and rodents. In humans, a linkage between remembering the past and imagining the future has been recognised. While chimpanzees can plan for the future, their episodic-like memory has hardly been investigated. We tested chimpanzees (Pan troglodytes) with an adapted food-catching paradigm. They observed the baiting of two locations amongst four and chose one after a given delay (15 min, 1 h or 5 h). We used two combinations of food types, a preferred and a less preferred food that disappeared at different rates. The subjects had to base their choices on the time elapsed since baiting, and on their memory of which food was where. They could recover either their preferred food or the one that remained present. All animals failed to obtain the preferred or present foods above chance levels. They were like-wise unsuccessful at choosing baited cups above chance levels. The subjects, thus, failed to use any feature of the baiting events to guide their choices. Nonetheless, their choices were not random, but the result of a developed location-based association strategy. Choices in the second half of the study correlated with the rewards obtained at each location in the first half of the study, independent from the choices made for each location in the first half of the study. This simple location-based strategy yielded a fair amount of food. The animals' failure to remember the what-where-when in the presented set-up may be due to the complexity of the task, rather than an inability to form episodic-like memories, as they even failed to remember what was where after 15 minutes.     

Daily, intermittent intravenous infusion of peptide YY(3-36) reduces daily food intake and adiposity in rats

The gut hormone peptide YY(3-36) [PYY(3-36)] decreases food intake when administered by intravenous infusion to lean and obese humans and rats. Whether chronic administration of PYY(3-36) produces a sustained reduction in food intake and adiposity is the subject of intense debate. Batterham et al. (R. L. Batterham, M. A. Cowley, C. J. Small, H. Herzog, M. A. Cohen, C. L. Dakin, A. M. Wren, A. E. Brynes, M. J. Low, M. A. Ghatei, R. D. Cone, and S. R. Bloom. Nature 418: 650-654, 2002) first reported that PYY(3-36) reduces food intake and weight gain in rats when injected into the peritoneal cavity twice daily for 7 days. Numerous laboratories have failed to confirm that daily injections of PYY(3-36) decrease body weight. Continuous subcutaneous administration of PYY(3-36) by osmotic minipump has been reported to reduce daily food intake in rodents but only during the first 3-4 days of administration. Here we show the effects of different daily patterns of intravenous infusion of PYY(3-36) on food intake, body weight, and adiposity in rats tethered via infusion swivels to computer-controlled pumps. Measurement of food bowl weight recorded by computer every 20 s permitted daily assessment of the instantaneous effects of PYY(3-36) administration on food intake and meal patterns. One-hour intravenous infusions of PYY(3-36) at 30 pmol x kg(-1) x min(-1) every other hour for 10 days produced a sustained reduction in daily food intake of approximately 20% and decreased body weight and adiposity by 7 and 35%, respectively. Thus dosage pattern is critical for producing a sustained effect of PYY(3-36) on food intake and adiposity.