Human-introduced long-term traditions in wild redfronted lemurs?

Behavioural traditions have only been described for a small subset of species, and the factors responsible for the maintenance of traditions over time are unclear. Redfronted lemurs are known to learn socially but traditions have not been described in the wild. We conducted a social diffusion experiment over three experimental years with artificial feeding boxes that could be opened in two different ways (pushing or pulling a door). Six out of 14 individuals that participated in at least 2 years exhibited a stable preference: five lemurs maintained a pull and one lemur a push preference, suggesting that habit formation and reinforcement learning may have lead to preferences over time. The remaining individuals exhibited fluctuating preferences and switched between showing a preference or no preference, but never switched between preferences. This instability might have been due to the low level of difficulty and/or the low object specificity of the task. The majority of lemurs additionally scrounged. Scrounging was not influenced by age, sex or success in manipulating the boxes. Thus, redfronted lemurs appear to use the two techniques flexibly but also scrounged opportunistically to get access to the rewards, indicating that traditions might be stabilized by multiple factors.     

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.     

Spatial memory in the grey mouse lemur (Microcebus murinus)

Wild animals face the challenge of locating feeding sites distributed across broad spatial and temporal scales. Spatial memory allows animals to find a goal, such as a productive feeding patch, even when there are no goal-specific sensory cues available. Because there is little experimental information on learning and memory capabilities in free-ranging primates, the aim of this study was to test whether grey mouse lemurs (Microcebus murinus), as short-term dietary specialists, rely on spatial memory in relocating productive feeding sites. In addition, we asked what kind of spatial representation might underlie their orientation in their natural environment. Using an experimental approach, we set eight radio-collared grey mouse lemurs a memory task by confronting them with two different spatial patterns of baited and non-baited artificial feeding stations under exclusion of sensory cues. Positional data were recorded by focal animal observations within a grid system of small foot trails. A change in the baiting pattern revealed that grey mouse lemurs primarily used spatial cues to relocate baited feeding stations and that they were able to rapidly learn a new spatial arrangement. Spatially concentrated, non-random movements revealed preliminary evidence for a route-based restriction in mouse lemur space; during a subsequent release experiment, however, we found high travel efficiency in directed movements. We therefore propose that mouse lemur spatial memory is based on some kind of mental representation that is more detailed than a route-based network map. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

On the function of redfronted lemur’s close calls

In order to maintain group cohesion, many social mammals and birds regularly produce close calls. In some primate species, close calls appear to have a dual function: calls addressed at a broad class of targets serve to maintain group cohesion, whereas the same calls directed at a specific target serve to regulate subsequent social interactions. Redfronted lemurs (Eulemur rufifrons) produce different types of close calls: grunts, long grunts, hoos and meows. In order to study the function of these calls, we conducted focal observations and vocal recordings from eight adult males and females out of four social groups in Kirindy Forest, Western Madagascar. Redfronted lemurs produce long grunts, hoos and meows at relatively low rates during foraging, resting or group movements, respectively. Grunts were given most often and more or less constantly during foraging and traveling. Calling rate increased when the risk of separation increased and may thus promote group cohesion. Grunts given during approaches of other group members resulted more often in friendly interactions than approaches that were not accompanied by a grunt. Thus, redfronted lemurs produce specific but also generic contact calls, whereas the latter calls have a dual function that varies depending on the addressed audience: they act as an auditory beacon to maintain group cohesion and serve as signals of benign intent to avoid costly conflicts and facilitating social interactions.     

Discriminative taste aversion learning: a learning task for older chickens

The study of learning and memory using the chicken model has relied on three learning paradigms, passive avoidance learning, imprinting and the pebble floor task. Passive avoidance learning and imprinting have been used predominantly in very young chickens and cannot be used to access learning and memory in older chickens. We have established a new behavioural learning paradigm, Discriminative Taste Aversion Learning (DTAL), that can be used with both young and older animals. The task requires chickens to discriminate between food crumbs dyed either red or yellow with one colour being associated with the aversive tasting substance, methylanthranilate. Learning can be tested at various times after the training session by presenting chickens with the coloured food crumbs without an aversive taste. Both chickens tested at 5 and 15 days post-hatch learned to avoid the aversive crumbs. Furthermore, the protein synthesis inhibitor anisomycin (30 mM; 10 microl per hemisphere) injected into the intermediate medial hyperstriatum ventrale 15 min pre-training or 45 min post-training blocked long-term memory for the DTAL task when tested 24 h later. Memory for the task was unaffected by anisomycin injection 120 min post-training or in control animals injected with saline at similar times. The timing of the cellular processes of protein synthesis needed for consolidation of the DTAL appears to be similar to those described for the other behavioural paradigms in young chickens.     

Ring-tailed lemurs (Lemur catta) exploit information about what others can see but not what they can hear

Studies suggest that haplorhine primates are sensitive to what others can see and hear. Using two experimental designs, we tested the hypothesis that ring-tailed lemurs (N = 16) are also sensitive to the visual and auditory perception of others. In the first task, we used a go/no–go design that required lemurs to exploit only auditory information. In the second task, we used a forced-choice design where lemurs competed against a human who would prevent them from obtaining food if their approaches were detected. Subjects were given the choice of obtaining food silently or noisily when the competitor’s back was turned. They were also given the choice to obtain food when the competitor could either see them or not. Here, we replicate the findings of previous studies indicating that ring-tailed lemurs are sensitive to whether they can be seen; however, we found no evidence that subjects are sensitive to whether others can hear them. Our findings suggest that ring-tailed lemurs converge with haplorhine primates only in their sensitivity to the visual information of others. The results emphasize the importance of investigating social cognition across sensory domains in order to elucidate the cognitive mechanisms that underlie apparently complex social behavior. These findings also suggest that the social dynamics of haplorhine groups impose greater cognitive demands than lemur groups, despite similarities in total group size.     

Posturally related variations in the hand preferences of the ruffed lemur (Varecia variegata variegata)

The hand preferences of 5 semi-free-ranging black-and-white ruffed lemurs were assessed by using three distinct testing procedures. Testing conditions varied in the extent to which they required animals to make a whole body postural adjustment prior to making a reach. Minimal bodily adjustment was necessary for free foraging, whereas discrete food presentations on land (DFP-land) and in a moat (DFP-moat) promoted a gross reorientation of the animal's entire body. In the DFP-moat condition 4 animals exhibited exclusive use of the left hand, and only 1 of 515 reaches was made with the right hand. Similarly, all 5 animals showed a pronounced left hand preference in the DFP-land condition. The free-foraging condition revealed a hand preference for only 1 of the 5 subjects, and that preference was weak in comparison with those measured in the other two test conditions. These findings indicate that whole body postural adjustments critically influenced the expression of hand preference and should be taken into consideration in future studies of primate hand preferences.     

The ecological rationality of delay tolerance: insights from capuchin monkeys

Both human and non-human animals often face decisions between options available at different times, and the capacity of delaying gratification has usually been considered one of the features distinguishing humans from other animals. However, this characteristic can widely vary across individuals, species, and types of task and it is still unclear whether it is accounted for by phylogenetic relatedness, feeding ecology, social structure, or metabolic rate. To disentangle these hypotheses, we evaluated temporal preferences in capuchin monkeys, South-American primates that, despite splitting off from human lineage approximately 35 million years ago, show striking behavioural analogies with the great apes. Then, we compared capuchins’ performance with that of the other primate species tested so far with the same procedure. Overall, capuchins showed a delay tolerance significantly higher than closely related species, such as marmosets and tamarins, and comparable to that shown by great apes. Capuchins’ tool use abilities might explain their comparatively high preference for delayed options in inter-temporal choices. Moreover, as in humans, capuchin females showed a greater delay tolerance than males, possibly because of their less opportunistic foraging style. Thus, our results shed light on the evolutionary origins of self-control supporting explanations of delay tolerance in terms of feeding ecology.     

Problem solving in great apes (Pan paniscus, Pan troglodytes, Gorilla gorilla, and Pongo abelii): the effect of visual feedback

What kind of information animals use when solving problems is a controversial topic. Previous research suggests that, in some situations, great apes prefer to use causally relevant cues over arbitrary ones. To further examine to what extent great apes are able to use information about causal relations, we presented three different puzzle box problems to the four nonhuman great ape species. Of primary interest here was a comparison between one group of apes that received visual access to the functional mechanisms of the puzzle boxes and one group that did not. Apes' performance in the first two, less complex puzzle boxes revealed that they are able to solve such problems by means of trial-and-error learning, requiring no information about the causal structure of the problem. However, visual inspection of the functional mechanisms of the puzzle boxes reduced the amount of time needed to solve the problems. In the case of the most complex problem, which required the use of a crank, visual feedback about what happened when the handle of the crank was turned was necessary for the apes to solve the task. Once the solution was acquired, however, visual feedback was no longer required. We conclude that visual feedback about the consequences of their actions helps great apes to solve complex problems. As the crank task matches the basic requirements of vertical string pulling in birds, the present results are discussed in light of recent findings with corvids.     

Diagnostic classification by experts and novices.

The present study examines differences between experts and novices in classifying symptoms and the effect of the nature of the task on classifying. The study involved three groups of subjects, two expert groups (n = 12, n = 10) and one novice group (n = 12). Thinking-aloud protocols were collected for two classification tasks: sorting of behavioural symptoms into predefined categories and intuitive clustering of behavioural symptoms. In a third task, experts and novices were asked to make typicality ratings of behavioural symptoms. The protocols were analyzed with respect to seven cognitive operations: (a) asking or giving information, (b) associating, (c) abstracting or labelling, (d) explaining, (e) neutral matching, (f) identifying, and (g) differentiating. Results showed an effect of experience and an effect of the task on the relative frequencies of these operations. No differences were found in typicality rating of experts versus novices. These contradictory findings are discussed in relation to Kolodner's model about the evolution of expertise.     

Object permanence in lemurs

Object permanence, the ability to mentally represent objects that have disappeared from view, should be advantageous to animals in their interaction with the natural world. The objective of this study was to examine whether lemurs possess object permanence. Thirteen adult subjects representing four species of diurnal lemur (Eulemur fulvus rufus, Eulemur mongoz, Lemur catta and Hapalemur griseus) were presented with seven standard Piagetian visible and invisible object displacement tests, plus one single visible test where the subject had to wait predetermined times before allowed to search, and two invisible tests where each hiding place was made visually unique. In all visible tests lemurs were able to find an object that had been in clear view before being hidden. However, when lemurs were not allowed to search for up to 25-s, performance declined with increasing time-delay. Subjects did not outperform chance on any invisible displacements regardless of whether hiding places were visually uniform or unique, therefore the upper limit of object permanence observed was Stage 5b. Lemur species in this study eat stationary foods and are not subject to stalking predators, thus Stage 5 object permanence is probably sufficient to solve most problems encountered in the wild.     

Knockdown of Nurr1 in the rat hippocampus: implications to spatial discrimination learning and memory

Nurr1 expression is up-regulated in the brain following associative learning experiences, but its relevance to cognitive processes remains unclear. In these studies, rats initially received bilateral hippocampal infusions of control or antisense oligodeoxynucleotides (ODNs) 1 h prior to training in a holeboard spatial discrimination task. Such pre-training infusions of nurr1 antisense ODNs caused a moderate effect in learning the task and also impaired LTM tested 7 d later. In a second experiment, ODN infusions were given immediately after the animals had received two sessions of training, during which all animals showed normal learning. Although antisense treated rats were significantly impaired during the post-infusion stages of acquisition of the task, no group differences were observed during the LTM test given 7 d later. These animals were subjected 3 d later to reversal training in the same maze in the absence of any additional treatments. Remarkably, rats previously treated with antisense ODNs displayed perseveration: The animals were fixated with the previously learned pattern of baited holes, causing them to be significantly impaired in the extinction of acquired spatial preferences and future learning. We postulate that Nurr1 function in the hippocampus is important for normal cognitive processes.     

Implicit sequence learning in ring‐tailed lemurs (Lemur catta)

Implicit learning involves picking up information from the environment without explicit instruction or conscious awareness of the learning process. In nonhuman animals, conscious awareness is impossible to assess, so we define implicit learning as occurring when animals acquire information beyond what is required for successful task performance. While implicit learning has been documented in some nonhuman species, it has not been explored in prosimian primates. Here we ask whether ring‐tailed lemurs (Lemur catta) learn sequential information implicitly. We tested lemurs in a modified version of the serial reaction time task on a touch screen computer. Lemurs were required to respond to any picture within a 2 × 2 grid of pictures immediately after its surrounding border flickered. Over 20 training sessions, both the locations and the identities of the images remained constant and response times gradually decreased. Subsequently, the locations and/or the identities of the images were disrupted. Response times indicated that the lemurs had learned the physical location sequence required in original training but did not learn the identity of the images. Our results reveal that ring‐tailed lemurs can implicitly learn spatial sequences, and raise questions about which scenarios and evolutionary pressures give rise to perceptual versus motor‐implicit sequence learning.     

Transfer of self-control in black (Eulemur macaco) and brown (Eulemur fulvus) lemurs: choice of a less preferred food item under a reverse-reward contingency

When presented a choice between two food-type arrays of equivalent size under a reverse-reward contingency, black (Eulemur macaco) and brown (Eulemur fulvus) lemurs transposed their self-control abilities, acquired in a previous experiment, to significantly select the less-desired food item in order to gain access to the more desired one. However, when presented with the choice between two different food-type arrays in which the amount of the less desired food array was larger than the more desired one, large individual differences were revealed: Some subjects established a consistent rule favoring quality or quantity, whereas others exhibited various point of trade-off. These results show that lemurs seem to manage the task considering not only food quantity but also food quality.     

Advice-taking as an unobtrusive measure of prejudice

A new unobtrusive measure of prejudice is proposed based on an advice-taking task. The computer-based task requires participants to find a token hidden behind one of two boxes. Prior to making their choice, however, someone (depicted by a name or a face) provides advice as to the token’s location. An unobtrusive measure of prejudice is derived by manipulating the advice-giver’s social group (e.g., male or female, Asian or White) and comparing the proportions of advice taken from each group. In Experiment 1, although the participants were not aware of it, they took more advice from males than from females. In Experiment 2, the relative proportion of advice taken from Asian versus White advice-givers correlated with responses to a news story pertaining to Asians. In Experiment 3, the relative proportion of advice taken from Asian versus White advice-givers correlated with scores on the Implicit Association Test (IAT) and predicted discriminatory behaviour, as indexed by the lost e-mail technique, better than other measures. In Experiment 4, scores on the advice task were uncontaminated by social desirability concerns and reactance and reflected the relative amounts of trust that people placed in different social groups. Taken together, these findings suggest that the advice task may be a useful tool for researchers seeking an unobtrusive measure of prejudice with predictive validity.     

Variance-sensitive choice in lemurs: constancy trumps quantity

Numerous studies have demonstrated that animals’ tolerance for risk when foraging can be affected by changes in metabolic state. Specifically, animals on a negative energy budget increase their preferences for risk, while animals on a positive energy budget are typically risk-averse. The malleability of these preferences may be evolutionarily advantageous, and important for maximizing chances of survival during brief periods of energetic stress. However, animals adapted to living in unpredictable conditions are unlikely to benefit from risk-seeking strategies, and instead are expected to reduce energetic demands while maintaining risk-aversion. We measured risk preferences in lemurs, a group of primates restricted to the island of Madagascar. Lemurs have evolved diverse anatomical and behavioral traits for survival in a harsh and unpredictable ecology, and these traits have been explained as forms of anatomical and behavioral risk reduction. We therefore predicted that lemurs would also be risk-averse in a behavioral task that offered subjects a choice between a small certain reward, and an uncertain but potentially large reward. In Experiment 1, the average rewards associated with the constant and variable options were equal and lemurs exhibited high levels of risk-aversion, replicating a phenomenon that has been demonstrated in dozens of taxa. In Experiment 2, we gradually increased the average value of the variable option relative to the constant option. Lemurs’ preferences tracked these changes and subjects became more risk-seeking as the risk premium increased. However, many subjects maintained high levels of risk-aversion even when the average payout of the variable option yielded double that of the constant option. These results are consistent with the notion that lemur cognition has evolved to minimize risk in an unpredictable island environment.     

Exploration and choice by mice among nest boxes differing in size: Influence of the inner and the outer dimensions

The size of nest boxes induces contrasting effects on exploratory behaviour and nest establishment of mice. Nest box exploration increases, and preference for nest site decreases, with increasing nest box size (Buhot, 1987). The aim of the present study was to continue the investigation of the different effects of the inner vs outer properties (here sizes) of nest boxes, the former being likely to play a major role in nest establishment, whereas the latter were predicted to be mainly involved in the initial exploratory process. The subjects were cagemate groups of two or three male mice. They were subjected to four ranking tests in which the nest boxes differed in outer size only, or in inner size only, and they either had a roof or did not have one. Among nest boxes with identical inside dimensions, the mice preferentially chose as nest sites those with the largest available outer dimensions; the presence of a roof did not affect this preference. In situations with nest boxes differing only in inner size, opposite preferences were observed, depending on whether or not a roof was present. In the presence of roofed nest boxes, mice's preferences were positively correlated with the size of the boxes. In the unroofed condition, an optimal value was observed around the second smaller inner-spaced nest box. Thus, both inner and outer properties influenced nest box choice. As a roof provides maximum safety, its presence seemed to have allowed choice to be governed by a secondary criterion—the maximum distance between the nest and the entrance. Initial exploration patterns were mainly influenced by the outer characteristics of the nest boxes: the larger the nest boxes were on the outside, the earlier and more frequently they were visited.     

Left hemispheric preference and alexithymia: A neuropsychological investigation

Starting from the hypothesis that alexithymics show a hyperactive left hemisphere, this study investigated the neural processing of visual information in two alexi-thymic groups and one nonalexithymic group. The subjects performed a lateralised visual-matching task, through which the proportions of ipsilateral and contralateral processing of three types of stimuli were assessed. In line with the hypothesis it was demonstrated that, in contradistinction to nonalexithymics, the two groups of alexithymics showed a left hemispheric preference in their neural processing of emotion words.     

Object individuation and labelling in 6-month-old infants

The ability to determine how many objects are involved in physical events is fundamental for reasoning about the world that surrounds us. Previous studies suggest that infants can fail to individuate objects in ambiguous occlusion events until their first birthday and that learning words for the objects may play a crucial role in the development of this ability. The present eye-tracking study tested whether the classical object individuation experiments underestimate young infants’ ability to individuate objects and the role word learning plays in this process. Three groups of 6-month-old infants (N = 72) saw two opaque boxes side by side on the eye-tracker screen so that the content of the boxes was not visible. During a familiarization phase, two visually identical objects emerged sequentially from one box and two visually different objects from the other box. For one group of infants the familiarization was silent (Visual Only condition). For a second group of infants the objects were accompanied with nonsense words so that objects’ shape and linguistic labels indicated the same number of objects in the two boxes (Visual & Language condition). For the third group of infants, objects’ shape and linguistic labels were in conflict (Visual vs. Language condition). Following the familiarization, it was revealed that both boxes contained the same number of objects (e.g. one or two). In the Visual Only condition, infants looked longer to the box with incorrect number of objects at test, showing that they could individuate objects using visual cues alone. In the Visual & Language condition infants showed the same looking pattern. However, in the Visual vs Language condition infants looked longer to the box with incorrect number of objects according to linguistic labels. The results show that infants can individuate objects in a complex object individuation paradigm considerably earlier than previously thought and that linguistic cues enforce their own preference in object individuation. The results are consistent with the idea that when language and visual information are in conflict, language can exert an influence on how young infants reason about the visual world.