Giraffes make decisions based on statistical information.

The ability to make inferences based on statistical information has so far been tested only in animals having large brains in relation to their body size, like primates and parrots. Here we tested if giraffes (Giraffa camelopardalis), despite having a smaller relative brain size, can rely on relative frequencies to predict sampling outcomes. We presented them with two transparent containers filled with different quantities of highly-liked food and less-preferred food. The experimenter covertly drew one piece of food from each container, and let the giraffe choose between the two options. In the first task, we varied the quantity and relative frequency of highly-liked and less-preferred food pieces. In the second task, we inserted a physical barrier in both containers, so giraffes only had to take into account the upper part of the container when predicting the outcome. In both tasks giraffes successfully selected the container more likely to provide the highly-liked food, integrating physical information to correctly predict sampling information. By ruling out alternative explanations based on simpler quantity heuristics and learning processes, we showed that giraffes can make decisions based on statistical inferences.

Innovation across 13 ungulate species: problem solvers are less integrated in the social group and less neophobic.

Innovation is the ability to solve new problems or find novel solutions to familiar problems, and it is known to provide animals with crucial fitness benefits. Although this ability has been extensively studied in some taxa, the factors that predict innovation within and across species are still largely unclear. In this study, we used a novel foraging task to test 111 individuals belonging to 13 ungulate species-a still understudied taxon. To solve the task, individuals had to open transparent and opaque cups with food rewards, by removing their cover. We assessed whether individual factors (neophobia, social integration, sex, age, rank) and socio-ecological factors (dietary breadth, fission-fusion dynamics, domestication, group size) predicted participation and performance in the task. Using a phylogenetic approach, we showed that success was higher for less neophobic and socially less integrated individuals. Moreover, less neophobic individuals, individuals of domesticated species and having higher fission-fusion dynamics were more likely to participate in the task. These results are in line with recent literature suggesting a central role of sociality and personality traits to successfully deal with novel challenges, and confirm ungulates as a promising taxon to test evolutionary theories with a comparative approach.

Neophobia in 10 ungulate species-a comparative approach.

ABSTRACT: Neophobia (the fearful reaction to novel stimuli or situations) has a crucial effect on individual fitness and can vary within and across species. However, the factors predicting this variation are still unclear. In this study, we assessed whether individual characteristics (rank, social integration, sex) and species socio-ecological characteristics (dietary breadth, group size, domestication) predicted variation in neophobia. For this purpose, we conducted behavioral observations and experimental tests on 78 captive individuals belonging to 10 different ungulate species-an ideal taxon to study inter-specific variation in neophobia given their variety in socio-ecological characteristics. Individuals were tested in their social groups by providing them with familiar food, half of which had been positioned close to a novel object. We monitored the individual latency to approach and eat food and the proportion of time spent in its proximity. Using a phylogenetic approach and social network analyses, we showed that across ungulate species neophobia was higher in socially more integrated individuals, as compared to less integrated ones. In contrast, rank and sex did not predict inter-individual differences in neophobia. Moreover, species differed in their levels of neophobia, with Barbary sheep being on average less neophobic than all the other study species. As group size in Barbary sheep was larger than in all the other study species, these results support the hypothesis that larger group size predicts lower levels of neophobia, and confirm ungulates as a highly promising taxon to study animal behavior and cognition with a comparative perspective. SIGNIFICANCE STATEMENT: In several species, individuals may respond fearfully to novel stimuli, therefore reducing the risks they may face. However, it is yet unclear if certain individuals or species respond more fearfully to novelty. Here, we provided food to 78 individual ungulates with different characteristics (e.g., sex, rank, social integration, group size, domestication, dietary breadth) in different controlled conditions (e.g., when food was close to novel or to familiar objects). Across species, we found that socially integrated individuals responded more fearfully in all species. Moreover, being in larger groups decreased the probability of fearfully responding to novelty. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00265-021-03041-0.

Comparative cognition in three understudied ungulate species: European bison, forest buffalos and giraffes.

BACKGROUND: Comparative cognition has historically focused on a few taxa such as primates, birds or rodents. However, a broader perspective is essential to understand how different selective pressures affect cognition in different taxa, as more recently shown in several studies. Here we present the same battery of cognitive tasks to two understudied ungulate species with different socio-ecological characteristics, European bison (Bison bonasus) and forest buffalos (Syncerus caffer nanus), and we compare their performance to previous findings in giraffes (Giraffa camelopardalis). We presented subjects with an Object permanence task, Memory tasks with 30 and 60 s delays, two inference tasks based on acoustic cues (i.e. Acoustic inference tasks) and a control task to check for the use of olfactory cues (i.e. Olfactory task). RESULTS: Overall, giraffes outperformed bison and buffalos, and bison outperformed buffalos (that performed at chance level). All species performed better in the Object permanence task than in the Memory tasks and one of the Acoustic inference tasks (which they likely solved by relying on stimulus enhancement). Giraffes performed better than buffalos in the Shake full Acoustic inference task, but worse than bison and buffalos in the Shake empty Acoustic inference task. CONCLUSIONS: In sum, our results are in line with the hypothesis that specific socio-ecological characteristics played a crucial role in the evolution of cognition, and that higher fission-fusion levels and larger dietary breadth are linked to higher cognitive skills. This study shows that ungulates may be an excellent model to test evolutionary hypotheses on the emergence of cognition.

Problem solving in European bison (Bison bonasus): two experimental approaches.

The ability to solve novel problems is crucial for individual fitness. However, studies on problem solving are usually done on few taxa, with species with low encephalization quotient being rarely tested. Here, we aimed to study problem solving in a non-domesticated ungulate species, European bison, with two experimental tasks. In the first task, five individuals were presented with a hanging barrel filled with food, which could either be directly accessed (control condition) or which could only be reached by pushing a tree stump in the enclosure below it and stepping on it (experimental condition). In the second task, five individuals were repeatedly fed by an experimenter using a novel bucket to retrieve food from a bag. Then, three identical buckets were placed in the enclosure, while the experimenter waited outside with the bag without feeding the bison, either with a bucket (control condition) or without it (experimental condition). In the first task, no bison moved the stump behind the barrel and/or stepped on it to reach the food. In the second task, two individuals solved the task by pushing the bucket within the experimenter's reach, twice in the experimental and twice in the control condition. We suggest that bison showed a limited ability to solve novel problems, and discuss the implications for their understanding of the functional aspects of the tasks.

Giraffes go for more: a quantity discrimination study in giraffes (Giraffa camelopardalis).

Many species, including humans, rely on an ability to differentiate between quantities to make decisions about social relationships, territories, and food. This study is the first to investigate whether giraffes (Giraffa camelopardalis) are able to select the larger of two sets of quantities in different conditions, and how size and density affect these decisions. In Task 1, we presented five captive giraffes with two sets containing a different quantity of identical foods items. In Tasks 2 and 3, we also modified the size and density of the food reward distribution. The results showed that giraffes (i) can successfully make quantity judgments following Weber's law, (ii) can reliably rely on size to maximize their food income, and (iii) are more successful when comparing sparser than denser distributions. More studies on different taxa are needed to understand whether specific selective pressures have favored the evolution of these skills in certain taxa.

Gaze Following in Ungulates: Domesticated and Non-domesticated Species Follow the Gaze of Both Humans and Conspecifics in an Experimental Context.

Gaze following is the ability to use others' gaze to obtain information about the environment (e.g., food location, predators, and social interactions). As such, it may be highly adaptive in a variety of socio-ecological contexts, and thus be widespread across animal taxa. To date, gaze following has been mostly studied in primates, and partially in birds, but little is known on the gaze following abilities of other taxa and, especially, on the evolutionary pressures that led to their emergence. In this study, we used an experimental approach to test gaze following skills in a still understudied taxon, ungulates. Across four species (i.e., domestic goats and lamas, and non-domestic guanacos and mouflons), we assessed the individual ability to spontaneously follow the gaze of both conspecifics and human experimenters in different conditions. In line with our predictions, species followed the model's gaze both with human and conspecific models, but more likely with the latter. Except for guanacos, all species showed gaze following significantly more in the experimental conditions (than in the control ones). Despite the relative low number of study subjects, our study provides the first experimental evidence of gaze following skills in non-domesticated ungulates, and contributes to understanding how gaze following skills are distributed in another taxon-an essential endeavor to identify the evolutionary pressures leading to the emergence of gaze following skills across taxa.

Bargaining in chimpanzees (Pan troglodytes): The effect of cost, amount of gift, reciprocity, and communication.

Humans routinely incur costs when allocating resources and reject distributions judged to be below/over an expected threshold. The dictator/ultimatum games (DG/UG) are two-player games that quantify prosociality and inequity aversion by measuring allocated distributions and rejection thresholds. Although the UG has been administered to chimpanzees and bonobos, no study has used both games to pinpoint their motivational substrate. We administered a DG/UG using preassigned distributions to four chimpanzee dyads controlling for factors that could explain why proposers' behavior varied substantially across previous studies: game order, cost for proposers, and amount for recipients. Moreover, players exchanged their roles (proposer/recipient) to test reciprocity. Our results show that proposers offered more in the DG than in the nonsocial baseline, particularly when they incurred no cost. In UG, recipients accepted all above-zero offers, suggesting absence of inequity aversion. Proposers preferentially chose options that gave larger amounts to the partner. However, they also decreased their offers across sessions, probably being inclined to punish their partner's rejections. Therefore, chimpanzees were not strategically motivated toward offering more generously to achieve ulterior acceptance from their partner. We found no evidence of reciprocity. We conclude that chimpanzees are generous rational maximizers that may not engage in strategic behavior. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

Object permanence in Giraffa camelopardalis: First steps in giraffes' physical cognition.

Although behavior, biology, and ecology of giraffes have been widely studied, little is known about their cognition. Giraffes' feeding ecology and their fission-fusion social dynamics are comparable with those of chimpanzees (Pan troglodytes), suggesting that they might have complex cognitive abilities. To assess this, we tested 6 captive giraffes on their object permanence, short-term memory, and ability to use acoustic cues to locate food. First, we tested whether giraffes understand that objects continue to exist even when they are out of sight. Giraffes saw one of two opaque containers containing food, then containers were closed, and 2 s later giraffes could choose one. Second, we measured giraffes' memory repeating the procedure but with a delay of 30 s, 60 s, or 2 min between closing the containers and subjects' choice. Finally, we investigated whether giraffes could locate food inside one of two identical opaque containers, when the only cue provided was the sound made by food when shaking the baited container, or the lack of sound when shaking the empty container. Our results show that giraffes form mental representations of completely hidden objects, but may not store them for longer than 30 s. Moreover, they rely on stimulus enhancement rather than acoustic cues to locate food, when no visual cues are provided. Finally, we argue that giraffes and other ungulates might be a suitable model to investigate the evolution of complex cognitive abilities from a comparative perspective. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

Vertical string-pulling in green jays (Cyanocorax yncas).

The cognition of green jays (Cyanocorax yncas), a non Corvus corvid species, was investigated by using the string-pulling paradigm. Five adult green jays performed a vertical string-pulling task in which they had to retrieve a worm attached to the end of a vertical hanging string while sitting on their perch. In the first experiment, three of the subjects managed to retrieve the worm by pulling on the string with their beaks and stepping on the resulting loop, and thereafter repeating this sequence until the worm was accessible. When subjects were given a choice between two strings in subsequent experiments 2-4, they chose at random between the string connected to the worm and the one connected to a slice of a wooden dowel. In experiment 5, subjects that had failed the previous discrimination series were able, nevertheless, to solve a more stringent vertical string array in which they had to pull up the whole length of the string without any visual access to the worm at the end. We discuss green jays' performance in comparison with other corvid species in which cognition has been more extensively investigated.

Do sex and age affect strategic behavior and inequity aversion in children?

The ultimatum game is commonly used to explore fairness in adults in bargaining situations. Although the changes in responses that occur during development have been investigated in children, the results have been mixed. Whereas some studies show that proposers offer more when they grow older, others indicate the opposite. Moreover, these studies are outcome-based and leave intentions out of the scene, although intentions play a relevant role in daily life. The mini-ultimatum game offers the opportunity to test both outcomes and intentions, but one major obstacle for accurately pinpointing developmental transitions in strategic behavior and inequity aversion so far has been the multiple confounds that have plagued previous studies, including different methods, small sample sizes, and reduced age differences. We administered an anonymous direct-method one-shot mini-ultimatum game to 478 6- and 10-year-old children. Strategic behavior was present at 10 years of age; older participants matched more accurately what responders would accept than younger participants. However, this was true only for older girls. No sex differences were detected in younger children. No age group seemed to consider the proposer's intentions given that the rejections of the default option were not significant across conditions. Both disadvantageous and advantageous inequity aversions were present in 6-year-olds. However, older children exhibited significantly more disadvantageous inequity aversion than younger children. This contrast made the pattern of rejection of 6-year-olds look more similar to the pattern of rejection found in adults. No sex differences were found in responders' behavior.

Population-level right-handedness for a coordinated bimanual task in naturalistic housed chimpanzees: replication and extension in 114 animals from Zambia and Spain.

Recently, many studies have been conducted on manual laterality in chimpanzees. Nevertheless, whether nonhuman primates exhibit population-level handedness remains a topic of considerable debate. One of the behaviors studied has been bimanual coordinated actions. Although recent studies have highlighted that captive chimpanzees show handedness at population level for these tasks, some authors have questioned the validity and consistency of these results. The first reason has been the humanization of the samples. The second one has been that the results refer to animals in American biomedical centers and the studies were conducted by the same team [WD Hopkins et al.]. This article aims to assess the laterality in bimanual coordination (tube task) activities in animals housed in an intermediate environment (Chimfunshi, Zambia). This has been conducted by replicating previous studies on similar samples (Mona Foundation, Spain), and then by extending the results to chimpanzees housed in intermediate settings. Individuals were evaluated through four experimental sessions (tests). Results indicated that 86% of the Chimfunshi sample was lateralized (48% RH, 38% LH). Furthermore, the sample showed population-level right-handedness in the mean handedness index, in Test 1, Test 2, and the first half of the study (Test 112). Rearing experience did not have an influence on handpreference. Taken together, the two sample (intermediate settings: Chimfunshi and Mona) results indicate a clear right-handedness. In conclusion, this replication and extension shows that (1) the Mona and Chimfunshi chimpanzees are right-handed in certain conditions, (2) the results are consistent with those obtained by Hopkins in captive settings, (3) the humanization of the samples does not affect manual laterality, (4) females are right-handed at population-level, but not males, and (5) these results reinforce the fact that the complexity of the task plays a dominant role in the expression of hand laterality among chimpanzees.

New evidence on imitation in an enculturated chimpanzee (Pan troglodytes).

Imitation in the great apes continues to be an active field of research and one that is not free of controversy. Several studies suggest that these species do not tend to match the motor movements of the model they observe, but try to achieve the same results using their own methods (emulation of results). In the studies reviewed, gestures have been used very infrequently outside an intraspecific communicative context to evaluate imitation. In fact, the imitation of gestural actions has been tested only in 4 individual great apes. This study assessed a chimpanzee's (Pan troglodytes) ability to imitate 52 actions in 4 categories. The levels of accuracy attained by the subject in her imitations exceeded those described in previous studies. Moreover, contrary to the idea defended in some articles, the subject seemed to find it easier to imitate gestures than actions with objects.

Another gorilla (Gorilla gorilla gorilla) recognizes himself in a mirror.

Various attempts have been made to explain why gorillas (Gorilla gorilla gorilla) find it difficult to recognize their mirror image. One of the most oft-cited reasons is aversion to eye contact, which stops gorillas from looking into a mirror and thus prevents them from carrying out a suitable exploration that could lead to self-recognition. In the experimental design used here the subject was first habituated both to observers and to the mirror as an object before being exposed to the latter. The study was performed with a single subject who was well adapted to captivity and exhibited no aberrant behavior or signs of stress. The results revealed that the subject had no aversion to eye contact. He showed considerable interest in the mirror and appeared relaxed when faced with his image. He gave a positive response to the mark test.

Mirror responses in a group of Miopithecus talapoin.

Studies of non-human primate self-recognition in mirrors demonstrate variation both within and between species. This study applied a rigorous methodology that took into account habituation of subjects to the mirror as an object and to the experimental situation. The species observed in our study was Miopithecus talapoin, which has been little studied in the wild or in captivity. Although this species shows several interesting characteristics, including complex social organisation and a high encephalization index, the talapoin monkeys in the study did not pass the mark test; however, they showed a prerequisite for self-recognition, namely comparing their body parts to the image of these in the mirror.