Inferences about the location of food in lemurs (Eulemur macaco and Eulemur fulvus): a comparison with apes and monkeys

The ability of black and brown lemurs (Eulemur macaco and Eulemur fulvus) to make inferences about hidden food was tested using the same paradigm as in Call’s (J Comp Psycol 118:232–241, 2004) cup task experiment. When provided with either visual or auditory information about the content of two boxes (one empty, one baited), lemurs performed better in the auditory condition than in the visual one. When provided with visual or auditory information only about the empty box, one subject out of four was above chance in the auditory condition, implying inferential reasoning. No subject was successful in the visual condition. This study reveals that (1) lemurs are capable of inferential reasoning by exclusion and (2) lemurs make better use of auditory than visual information. The results are compared with the performances recorded in apes and monkeys under the same paradigm.     

Capuchin monkeys (Cebus apella) use positive, but not negative, auditory cues to infer food location

Nonhuman primates appear to capitalize more effectively on visual cues than corresponding auditory versions. For example, studies of inferential reasoning have shown that monkeys and apes readily respond to seeing that food is present (“positive” cuing) or absent (“negative” cuing). Performance is markedly less effective with auditory cues, with many subjects failing to use this input. Extending recent work, we tested eight captive tufted capuchins (Cebus apella) in locating food using positive and negative cues in visual and auditory domains. The monkeys chose between two opaque cups to receive food contained in one of them. Cup contents were either shown or shaken, providing location cues from both cups, positive cues only from the baited cup, or negative cues from the empty cup. As in previous work, subjects readily used both positive and negative visual cues to secure reward. However, auditory outcomes were both similar to and different from those of earlier studies. Specifically, all subjects came to exploit positive auditory cues, but none responded to negative versions. The animals were also clearly different in visual versus auditory performance. Results indicate that a significant proportion of capuchins may be able to use positive auditory cues, with experience and learning likely playing a critical role. These findings raise the possibility that experience may be significant in visually based performance in this task as well, and highlight that coming to grips with evident differences between visual versus auditory processing may be important for understanding primate cognition more generally.     

Inferences about the location of food in the great apes (Pan paniscus, Pan troglodytes, Gorilla gorilla, and Pongo pygmaeus)

Bonobos (Pan paniscus; n = 4), chimpanzees (Pan troglodytes; n = 12), gorillas (Gorilla gorilla; n = 8), and orangutans (Pongo pygmaeus; n = 6) were presented with 2 cups (1 baited) and given visual or auditory information about their contents. Visual information consisted of letting subjects look inside the cups. Auditory information consisted of shaking the cup so that the baited cup produced a rattling sound. Subjects correctly selected the baited cup both when they saw or heard the food. Nine individuals were above chance in both visual and auditory conditions. More important, subjects as a group selected the baited cup when only the empty cup was either shown or shaken, which means that subjects chose correctly without having seen or heard the food (i.e., inference by exclusion). Control tests showed that subjects were not more attracted to noisy cups, avoided shaken noiseless cups, or learned to use auditory information as a cue during the study. It is concluded that subjects understood that the food caused the noise, not simply that the noise was associated with the food.     

Tool choice on the basis of rigidity in capuchin monkeys

Wild capuchin monkeys select stone tools to crack open nuts on the basis of their weight and friability, two non-visual functional properties. Here, we investigated whether they would select new stick-like tools on the basis of their rigidity. In Experiment 1, subjects faced an out-of-reach reward and a choice of three unfamiliar tools differing in color, diameter, material, and rigidity. In order to retrieve the reward, capuchins needed to select the rigid tool exemplar. Capuchins gathered information regarding tools’ pliability either by (1) manipulating the tools themselves (manipulation condition), (2) observing a human demonstrator repeatedly bending the tools (observation condition), or (3) seeing the tools placed on a platform without any manipulation taking place (visual static condition). Subjects selected the rigid tool above chance levels in both the manipulation and observation conditions, but not in the visual static condition. In Experiment 2, subjects needed to select and use a flexible tool to access a liquid reward (as opposed to the rigid tool, as in previous experiment). Again, capuchins selected above chance levels the appropriate tool (i.e., flexible), thus demonstrating a good appreciation of the relation between the tool properties and the task requirements.     

Inferential reasoning by exclusion in children (Homo sapiens)

The cups task is the most widely adopted forced-choice paradigm for comparative studies of inferential reasoning by exclusion. In this task, subjects are presented with two cups, one of which has been surreptitiously baited. When the empty cup is shaken or its interior shown, it is possible to infer by exclusion that the alternative cup contains the reward. The present study extends the existing body of comparative work to include human children (Homo sapiens). Like chimpanzees (Pan troglodytes) that were tested with the same equipment and near-identical procedures, children aged three to five made apparent inferences using both visual and auditory information, although the youngest children showed the least-developed ability in the auditory modality. However, unlike chimpanzees, children of all ages used causally irrelevant information in a control test designed to examine the possibility that their apparent auditory inferences were the product of contingency learning (the duplicate cups test). Nevertheless, the children's ability to reason by exclusion was corroborated by their performance on a novel verbal disjunctive syllogism test, and we found preliminary evidence consistent with the suggestion that children used their causal-logical understanding to reason by exclusion in the cups task, but subsequently treated the duplicate cups information as symbolic or communicative, rather than causal. Implications for future comparative research are discussed.     

Inferential reasoning by exclusion in great apes, lesser apes, and spider monkeys

Using the cups task, in which subjects are presented with limited visual or auditory information that can be used to deduce the location of a hidden reward, Call (2004) found prima facie evidence of inferential reasoning by exclusion in several great ape species. One bonobo (Pan paniscus) and two gorillas (Gorilla gorilla) appeared to make such inferences in both the visual and auditory domains. However, common chimpanzees (Pan troglodytes) were successful only in the visual domain, and Bornean orangutans (Pongo pygmaeus) in neither. The present research built on this paradigm, and Experiment 1 yielded prima facie evidence of inference by exclusion in both domains for two common chimpanzees, and in the visual domain for two Sumatran orangutans (Pongo abelii). Experiments 2 and 3 demonstrated that two specific associative learning explanations could not readily account for these results. Because an important focus of the program of research was to assess the cognitive capacities of lesser apes (family Hylobatidae), we modified Call's original procedures to better suit their attentional and dispositional characteristics. In Experiment 1, testing was also attempted with three gibbon genera (Symphalangus, Nomascus, Hylobates), but none of the subjects completed the standard task. Further testing of three siamangs (Symphalangus syndactylus) and a spider monkey (Ateles geoffroyi) using a faster method yielded prima facie evidence of inferential reasoning by exclusion in the visual domain among the siamangs (Experiment 4).     

Under what conditions do young children have difficulty inhibiting manual actions?

Understanding how responses become prepotent is essential for understanding when inhibitory control is needed in everyday behavior. The authors investigated the conditions under which manual actions became prepotent in a go/no-go task. Children had to open boxes that contained stickers on go trials and leave shut boxes that were empty on no-go trials. In Experiment 1 (n = 40, mean age = 3.6 years), the authors obtained evidence consistent with this task requiring inhibitory control. Results of Experiment 2 (n = 40, mean age = 3.7 years) suggested that box opening was prepotent because (a) opening is the habitual action associated with boxes and (b) children planned to open boxes on go trials of the task. Experiment 3 (n = 96, mean age = 3.5 years) showed that even empty boxes elicited the same errors and that delaying responding reduced errors even though the delay occurred before the cue that indicated the correct response (contrary to a rule reflection account). Because the delay occurred after box presentation, performance was consistent with a transient activation account. Delay training might benefit children with weak inhibition.     

How do symbols affect 3‐ to 4‐year‐olds' executive function? Evidence from a reverse‐contingency task

In two experiments, 330 3‐ to 4‐year‐olds competed for stickers in a game in which the optimal response strategy was to point to an empty box that their opponent would receive in order to obtain a baited box for themselves. When the baited box contained stickers, children showed a strong tendency to point at the baited box and therefore lose the stickers to their opponent. In Experiment 1 children performed better when the number of stickers to be won was represented with one of five different types of symbol: numerals, number words, dots, a photograph or sweets. In Experiment 2 children transferred their improved performance in symbolic conditions to non‐symbolic conditions. These findings suggest that symbols enable children to formulate an efficient response strategy, and that this effect may be qualitatively different in children from the effect of symbols in non‐human primates.     

Duration discrimination of empty and filled intervals marked by auditory and visual signals

Experiments 1 and 2 compared, with a single-stimulus procedure, the discrimination of filled and empty intervals in both auditory and visual modalities. In Experiment 1, in which intervals were about 250 msec, the discrimination was superior with empty intervals in both modalities. In Experiment 2, with intervals lasting about 50 msec, empty intervals showed superior performance with visual signals only. In Experiment 3, for the auditory modality at 250 msec, the discrimination was easier with empty intervals than with filled intervals with both the forced-choice (FC) and the single stimulus (SS) modes of presentation, and the discrimination was easier with the FC than with the SS method. Experiment 4, however, showed that at 50 and 250 msec, with a FC-adaptive procedure, there were no differences between filled and empty intervals in the auditory mode; the differences observed with the visual mode in Experiments 1 and 2 remained significant. Finally, Experiment 5 compared differential thresholds for four marker-type conditions, filled and empty intervals in the auditory and visual modes, for durations ranging from .125 to 4 sec. The results showed (1) that the differential threshold differences among marker types are important for short durations but decrease with longer durations, and (2) that a generalized Weber’s law generally holds for these conditions. The results as a whole are discussed in terms of timing mechanisms.     

Redundant food searches by capuchin monkeys (Cebus apella): a failure of metacognition?

This study investigated capuchin monkeys' understanding of their own visual search behavior as a means to gather information. Five monkeys were presented with three tubes that could be visually searched to determine the location of a bait. The bait's visibility was experimentally manipulated, and the monkeys' spontaneous visual searches before tube selection were analyzed. In Experiment 1, three monkeys selected the baited tube significantly above chance; however, the monkeys also searched transparent tubes. In Experiment 2, a bent tube in which food was never visible was introduced. When the bent tube was baited, the monkeys failed to deduce the bait location and responded randomly. They also continued to look into the bent tube despite not gaining any pertinent information from it. The capuchin monkeys' behavior contrasts with the efficient employment of visual search behavior reported in humans, apes and macaques. This difference is consistent with species-related variations in metacognitive abilities, although other explanations are also possible.     

A comparison of the effects of spatial separation on apparent motion in the auditory and visual modalities

In the present investigation, the effects of spatial separation on the interstimulus onset intervals (ISOIs) that produce auditory and visual apparent motion were compared. In Experiment 1, subjects were tested on auditory apparent motion. They listened to 50-msec broadband noise pulses that were presented through two speakers separated by one of six different values between 0 degrees and 160 degrees. On each trial, the sounds were temporally separated by 1 of 12 ISOIs from 0 to 500 msec. The subjects were instructed to categorize their perception of the sounds as "single," "simultaneous," "continuous motion," "broken motion," or "succession." They also indicated the proper temporal sequence of each sound pair. In Experiments 2 and 3, subjects were tested on visual apparent motion. Experiment 2 included a range of spatial separations from 6 degrees to 80 degrees; Experiment 3 included separations from .5 degrees to 10 degrees. The same ISOIs were used as in Experiment 1. When the separations were equal, the ISOIs at which auditory apparent motion was perceived were smaller than the values that produced the same experience in vision. Spatial separation affected only visual apparent motion. For separations less than 2 degrees, the ISOIs that produced visual continuous motion were nearly equal to those which produced auditory continuous motion. For larger separations, the ISOIs that produced visual apparent motion increased.     

Is caching the key to exclusion in corvids? The case of carrion crows (Corvus corone corone)

Recently, two corvid species, food-caching ravens and non-caching jackdaws, have been tested in an exclusion performance (EP) task. While the ravens chose by exclusion, the jackdaws did not. Thus, foraging behaviour may affect EP abilities. To investigate this possibility, another food-caching corvid species, the carrion crow (Corvus corone corone), was tested in the same exclusion task. We hid food under one of two cups and subsequently lifted either both cups, or the baited or the un-baited cup. The crows were significantly above chance when both cups were lifted or when only the baited cup was lifted. When the empty cup was lifted, we found considerable inter-individual variation, with some birds having a significant preference for the un-baited but manipulated cup. In a follow-up task, we always provided the birds with the full information about the food location, but manipulated in which order they saw the hiding or the removal of food. Interestingly, they strongly preferred the cup which was manipulated last, even if it did not contain any food. Therefore, we repeated the first experiment but controlled for the movement of the cups. In this case, more crows found the food reliably in the un-baited condition. We conclude that carrion crows are able to choose by exclusion, but local enhancement has a strong influence on their performance and may overshadow potential inferential abilities. However, these findings support the hypothesis that caching might be a key to exclusion in corvids.     

Use of visual, acoustic, and olfactory information during embedded invertebrate foraging in brown capuchins (Cebus apella)

Experiments were conducted to investigate which sensory cues are used by brown capuchins (Cebus apella) in embedded invertebrate foraging. The importance of visual, olfactory, and acoustic cues in such foraging was determined by presenting subjects with a stimulus log modified to block out given sensory cues. Experiment 1 was designed to investigate whether subjects could locate an invertebrate embedded in wood when only visual, acoustic, or olfactory information was available. Experiments 2 and 3 were designed to investigate extractive foraging behavior when two sensory cues were provided. It was hypothesized that the combination of visual and acoustic information would be necessary for subjects to successfully locate embedded invertebrates. Results indicated that subjects' performance was most successful when both visual and acoustic information was available.     

Numerical competence in rats (Rattus norvegicus): Davis and Bradford (1986) extended

The task of rats (Rattus norvegicus) was to enter 1 box of a defined ordinal number among an array of boxes. In Experiments 1 and 2, the rats correctly chose the 4th box from arrays of 6 and 12 boxes, respectively. In Experiments 3 and 4, in which the ordinal number of the correct box was increased in a graduated fashion, they were able to select the correct box even when its position was higher than 10th among 12 and 18 boxes, respectively. In Experiment 5, the possibility that the rats had used cues to the openability of the box doors was ruled out. In Experiments 6 and 7, the rats succeeded in the task even when the total number of boxes was varied from trial to trial. In Experiment 8, both small- and large-sized boxes were used to control for the possibility of using the cumulative length of the boxes as a cue. Overall, the results suggest that performance was based on numerical cues. Intentional acts were occasionally observed but appeared not to be essential for solving the task.     

Testing a stochastic foraging model in an operant simulation: Agreement with qualitative but not quantitative predictions

An operant simulation of foraging through baited and empty patches was studied with 4 pigeons. On a three-key panel, side keys were designated as patches, and successive opportunities to complete 16 fixed-ratio 10 schedules on side keys were defined as encounters with feeders. In a random half of the patches in any session, some of the fixed-ratio 10 schedules yielded reinforcement (baited feeders) and the other schedules yielded nonreinforcement (empty feeders). In the other half of the patches, all feeders were empty. Pigeons could travel between patches at any time by completing a fixed-ratio schedule on the center key. An optimal foraging model was tested in Experiments 1 and 2 by varying center-key travel time and number of baited feeders in baited patches. The ordinal predictions that number of feeders visited in empty patches would increase with travel time and decrease as number of baited feeders increased were supported, but pigeons visited far more feeders in empty patches than the optimal number predicted by the model to maximize energy/time. In Experiment 3, evidence was found to suggest that the number of empty feeders encountered before the first baited feeder in baited patches is an important factor controlling leaving empty patches.     

Inferences by exclusion in the great apes: the effect of age and species

This study investigated the ability of chimpanzees, gorillas, orangutans, and bonobos to make inferences by exclusion using the procedure pioneered by Premack and Premack (Cognition 50:347–362, 1994) with chimpanzees. Thirty apes were presented with two different food items (banana vs. grape) on a platform and covered with identical containers. One of the items was removed from the container and placed between the two containers so that subjects could see it. After discarding this item, subjects could select between the two containers. In Experiment 1, apes preferentially selected the container that held the item that the experimenter had not discarded, especially if subjects saw the experimenter remove the item from the container (but without seeing the container empty). Experiment 3 in which the food was removed from one of the containers behind a barrier confirmed these results. In contrast, subjects performed at chance levels when a stimulus (colored plastic chip: Exp. 1; food item: Exp. 2 and Exp. 3) designated the item that had been removed. These results indicated that apes made inferences, not just learned to use a discriminative cue to avoid the empty container. Apes perceived and treated the item discarded by the experimenter as if it were the very one that had been hidden under the container. Results suggested a positive relationship between age and inferential ability independent of memory ability but no species differences.This contribution is part of the special issue “Animal Logics” (Watanabe and Huber 2006).     

Do chimpanzees (Pan troglodytes) and 2-year-old children (Homo sapiens) understand double invisible displacement?

Chimpanzees (Pan troglodytes) and young children (Homo sapiens) have difficulty with double invisible displacements in which an object is hidden in two nonadjacent boxes in a linear array. Experiment 1 eliminated the possibility that chimpanzees' previous poor performance was due to the hiding direction of the displacement device. As in Call (2001), subjects failed double nonadjacent displacements, showing a tendency to select adjacent boxes. In Experiments 2 and 3, chimpanzees and 24-month-old children were tested on a new adaptation of the task in which four hiding boxes were presented in a diamond-shaped array on a vertical plane. Both species performed above chance on double invisible displacements using this format, suggesting that previous poor performance was due to a response bias or inhibition problem rather than a fundamental limitation in representational capacity.     

Let's Make a Deal: Quality and availability of second-stage information as a catalyst for change

The Monty Hall Problem (MHP), a process of two-stage decision making, was presented in atypical form via a custom software game. Differing from the normal three-box MHP, the game added one additional box on-screen for each game—culminating on game 23 with 25 on-screen boxes to initially choose from. A total of 108 participants played 23 games (trials) in one of four conditions; (1) “Vanish” condition—all non-winning boxes totally removed from the screen; (2) “Empty” condition—all non-winning boxes remain on-screen, but with an “empty” label on them; (3) “Steroids” condition—all non-winning boxes removed from the screen, with initially chosen box becoming 25% larger; (4) “Steroids2” condition—all non-winning boxes removed from the screen, box not currently chosen becomes 25% larger. Results indicate second-stage on-screen presence of boxes influences switching; with their absence having the opposite effect. Size manipulation appears to elicit demand characteristics resulting in indeterminate influence.     

Modality-specific coding in matching letters

Auditory and visual similarity was manipulated in a same-different reaction-time task to investigate the use of modality-specific codes in same-different judgments for pairs of letters. Experiment 1 showed that letters presented simultaneously in the auditory and visual modalities were matched on the auditory dimension. In Experiment 2, the letters were presented sequentially, and the modality of the second letter was randomly varied. Subjects matched the pairs on the modality dimension of the second letter even though the modality could not be reliably predicted. In Experiment 3, subjects judged adjacent pairs of letters presented for 50 msec, and in one condition they also named the letters. Matches were made on visual codes in both conditions. In general, the results indicate that when subjects are instructed to determine if two letters are the same, the letters will be matched on a modality-specific code in a way that will minimize the information processing necessary to complete the match.     

Incidental memory in dogs (Canis familiaris): adaptive behavioral solution at an unexpected memory test

Memory processing in nonhuman animals has been typically tested in situations where the animals are repeatedly trained to retrieve their memory trace, such as delayed matching to sample, serial probe recognition, etc. In contrast, how they utilize incidentally formed memory traces is not well investigated except in rodents. We examined whether domestic dogs could solve an unexpected test based on a single past experience. In Experiment 1, leashed dogs were led to 4 open, baited containers and allowed to eat from 2 of them (Exposure phase). After a walk outside for more than 10?min, during which time the containers were replaced with new identical ones, the dogs were unexpectedly returned to the site and unleashed for free exploration (test phase). Eleven out of 12 dogs first visited one of the containers from which they had not eaten. In Experiment 2, two containers had food in them, one had a nonedible object, and the last one was empty. Dogs visited all 4 containers and were allowed to eat one of the food rewards in the Exposure phase. In the test phase, unleashed dogs first visited the previously baited container from which they had not eaten significantly more often than chance. These results demonstrate that in an unexpected, test dogs may retrieve “what” and “where” information about seen (now invisible) items from incidental memory formed during a single past experience.