Does opportunistic testing bias cognitive performance in primates? Learning from drop-outs

Dropouts are a common issue in cognitive tests with non-human primates. One main reason for dropouts is that researchers often face a trade-off between obtaining a sufficiently large sample size and logistic restrictions, such as limited access to testing facilities. The commonly-used opportunistic testing approach deals with this trade-off by only testing those individuals who readily participate and complete the cognitive tasks within a given time frame. All other individuals are excluded from further testing and data analysis. However, it is unknown if this approach merely excludes subjects who are not consistently motivated to participate, or if these dropouts systematically differ in cognitive ability. If the latter holds, the selection bias resulting from opportunistic testing would systematically affect performance scores and thus comparisons between individuals and species. We assessed the potential effects of opportunistic testing on cognitive performance in common marmosets (Callithrix jacchus) and squirrel monkeys (Saimiri sciureus) with a test battery consisting of six cognitive tests: two inhibition tasks (Detour Reaching and A-not-B), one cognitive flexibility task (Reversal Learning), one quantity discrimination task, and two memory tasks. Importantly, we used a full testing approach in which subjects were given as much time as they required to complete each task. For each task, we then compared the performance of subjects who completed the task within the expected number of testing days with those subjects who needed more testing time. We found that the two groups did not differ in task performance, and therefore opportunistic testing would have been justified without risking biased results. If our findings generalise to other species, maximising sample sizes by only testing consistently motivated subjects will be a valid alternative whenever full testing is not feasible.</p

How task format affects cognitive performance:a memory test with two species of New World monkeys

In cognitive tests, animals are often given a choice between two options and obtain a reward if they choose correctly. We investigated whether task format affects subjects' performance in a physical cognition test. In experiment 1, a two-choice memory test, 15 marmosets, Callithrix jacchus, had to remember the location of a food reward over time delays of increasing duration. We predicted that their performance would decline with increasing delay, but this was not found. One possible explanation was that the subjects were not sufficiently motivated to choose correctly when presented with only two options because in each trial they had a 50% chance of being rewarded. In experiment 2, we explored this possibility by testing eight naïve marmosets and seven squirrel monkeys, Saimiri sciureus, with both the traditional two-choice and a new nine-choice version of the memory test that increased the cost of a wrong choice. We found that task format affected the monkeys' performance. When choosing between nine options, both species performed better and their performance declined as delays became longer. Our results suggest that the two-choice format compromises the assessment of physical cognition, at least in memory tests with these New World monkeys, whereas providing more options, which decreases the probability of obtaining a reward when making a random guess, improves both performance and measurement validity of memory. Our findings suggest that two-choice tasks should be used with caution in comparisons within and across species because they are prone to motivational biases

Cognitive consequences of cooperative breeding in primates?

Several hypotheses propose that cooperative breeding leads to increased cognitive performance, in both nonhuman and human primates, but systematic evidence for such a relationship is missing. A causal link might exist because motivational and cognitive processes necessary for the execution and coordination of helping behaviors could also favor cognitive performance in contexts not directly related to caregiving. In callitrichids, which among primates rely most strongly on cooperative breeding, these motivational and cognitive processes include attentional biases toward monitoring others, the ability to coordinate actions spatially and temporally, increased social tolerance, increased responsiveness to others' signals, and spontaneous prosociality. These processes are likely to enhance performance particularly in socio-cognitive contexts. Therefore, cooperatively breeding primates are expected to outperform their independently breeding sister taxa in socio-cognitive tasks. We evaluate this prediction by reviewing the literature and comparing cognitive performance in callitrichids with that of their sister taxa, i.e. squirrel monkeys, which are independent breeders, and capuchin monkeys, which show an intermediate breeding system. Consistent with our prediction, this review reveals that callitrichids systematically and significantly outperform their sister taxa in the socio-cognitive, but not in the non-social domain. This comparison is complemented with more qualitative evaluations of prosociality and cognitive performance in non-primate cooperative breeders, which suggest that among mammals, cooperative breeding generally produces conditions conducive to socio-cognitive performance. In the hominid lineage, however, the adoption of extensive allomaternal care presumably resulted in more pervasive cognitive consequences, because the motivational consequences of cooperative breeding was added to an ape-level cognitive system already capable of understanding simple mental states, which enabled the emergence of shared intentionalit

An evaluation of the geographic method for recognizing innovations in nature, using zoo orangutans

Innovation and social learning are the raw materials for traditions and culture. Of these two, innovation has received far less scrutiny, largely because of difficulties assessing the innovation status of behaviors. A recent attempt proposes recognition of innovations in natural populations based on assessment of the behavior's properties and its geographic and local prevalence. Here we examine the validity of this approach and the list of 43 potential innovations it generated for wild orangutans by extending the comparison to zoo orangutans. First, we created an inventory of the behavioral repertoire in the zoo population. Four of ten putative innovations recognized in the field and potentially present in captivity did not occur despite appropriate conditions, suggesting they are indeed innovations. Second, we experimentally produced relevant conditions to evaluate whether another five potential innovations could be elicited. Based on their continued absence or on their latencies relative to known behaviors, four of the potential innovations could be assessed as innovations and one as a modification. Because 53% of relevant innovations recognized in the field could be confirmed in this analysis, and another 27% assigned possible innovation status, we conclude that the geographic method for detecting innovation in the wild is valid. However, the experiments also yielded up to 13 additional innovations, suggesting that zoo orangutans are far more innovative than wild ones. We discuss the implications of this latter finding with regard to limiting factors for the expansion of cultural repertoires in wild orangutan

No evidence for general intelligence in a fish

The average mammal or bird has a roughly ten times larger brain relative to body size than the average ectotherm vertebrate. It has been surprisingly challenging to determine how this translates into increased cognitive performance. In particular, it is unclear whether the brain size differences translate into qualitative differences in specific cognitive abilities. Here, we provide a first exploratory study to examine the possibility that the larger brains of endotherms support a different organisation of information processing, rather than specific differences in cognitive processes. In mammals, individual performance across domain-general cognitive tasks is positively correlated, resulting in the psychometric factor g. The value of g is positively correlated with brain size. We tested wild-caught female cleaner fish Labroides dimidiatus, known for its highly sophisticated social behaviour, in four ecologically nonrelevant cognitive tasks that have been used to varying degrees to assess g in mammals. Cleaner fish solved three of these four tasks, flexibility (reversal learning), self-control (detour around an obstacle) and numerical competence (simultaneous two-choice task), while also providing enough interindividual variation to test for g. They did not perform above chance levels in the fourth task, which tested for object permanence. For the three retained tasks, individual performance did not load positively on one principal component. Furthermore, all pairwise correlation coefficients were close to zero. These negative results contradict a frequent criticism of g studies, which proposes that g is a default result of how brains are designed. Rather, the results provide a first indication that endotherm and ectotherm vertebrates may process cognitive tasks in fundamentally different ways due to differences in brain organisation. Our relatively low number of experiments compared to mammalian studies enhances this hypothesis, as the probability of finding a g factor by chance would have been higher

The Antihero in the Novels of Juan Antonio de Zunzunegui

Although some of Zunzunegui's works are not so moralistic in intent as others, it will be seen that each one of them criticizes a particular bad trait in the protagonist which leads to unhappiness or defeat, either for the character himself or for someone close to him

Evolutionary precursors of social norms in chimpanzees: a new approach

Moral behaviour, based on social norms, is commonly regarded as a hallmark of humans. Hitherto, humans are perceived to be the only species possessing social norms and to engage in moral behaviour. There is anecdotal evidence suggesting their presence in chimpanzees, but systematic studies are lacking. Here, we examine the evolution of human social norms and their underlying psychological mechanisms. For this, we distinguish between conventions, cultural social norms and universal social norms. We aim at exploring whether chimpanzees possess evolutionary precursors of universal social norms seen in humans. Chimpanzees exhibit important preconditions for their presence and enforcement: tolerant societies, well-developed social-cognitive skills and empathetic competence. Here, we develop a theoretical framework for recognizing different functional levels of social norms and distinguish them from mere statistical behavioural regularities. Quasi social norms are found where animals behave functionally moral without having moral emotions. In proto social norms, moral emotions might be present but cannot be collectivized due to the absence of a uniquely human psychological trait, i.e. shared intentionality. Human social norms, whether they are universal or cultural, involve moral emotions and are collectivized. We will discuss behaviours in chimpanzees that represent potential evolutionary precursors of human universal social norms, with special focus on social interactions involving infants. We argue that chimpanzee infants occupy a special status within their communities and propose that tolerance towards them might represent a proto social norm. Finally, we discuss possible ways to test this theoretical framewor

From sharing food to sharing information: Cooperative breeding and language evolution

Language is a cognitively demanding human trait, but it is also a fundamentally cooperative enterprise that rests on the motivation to share information. Great apes possess many of the cognitive prerequisites for language, but largely lack the motivation to share information. Callitrichids (including marmosets and tamarins) are highly vocal monkeys that are more distantly related to humans than great apes are, but like humans, they are cooperative breeders and all group members help raising offspring. Among primates, this rearing system is correlated with proactive prosociality, which can be expressed as motivation to share information. We therefore propose that the unique coincidence of these two components in humans set the stage for language evolution: The cognitive component inherited from our great ape-like ancestors, and the motivational one added convergently as a result of cooperative breeding. We evaluate this scenario based on a review of callitrichd vocal communication and show that furthermore, they possess many of the mechanistic elements emphasized by the mirror system hypothesis of language evolution. We end by highlighting how more systematic phylogenetic comparisons will enable us to further promote our understanding of the role of cooperative breeding during language evolution

Optimising source identification from marmoset vocalisations with hierarchical machine learning classifiers

Marmosets, with their highly social nature and complex vocal communication system, are important models for comparative studies of vocal communication and, eventually, language evolution. However, our knowledge about marmoset vocalisations predominantly originates from playback studies or vocal interactions between dyads, and there is a need to move towards studying group-level communication dynamics. Efficient source identification from marmoset vocalisations is essential for this challenge, and machine learning algorithms (MLAs) can aid it. Here we built a pipeline capable of plentiful feature extraction, meaningful feature selection, and supervised classification of vocalisations of up to 18 marmosets. We optimised the classifier by building a hierarchical MLA that first learned to determine the sex of the source, narrowed down the possible source individuals based on their sex, and then determined the source identity. We were able to correctly identify the source individual with high precisions (87.21% – 94.42%, depending on call type, and up to 97.79% after the removal of twins from the dataset). We also examine the robustness of identification across varying sample sizes. Our pipeline is a promising tool not only for source identification from marmoset vocalisations but also for analysing vocalisations and tracking vocal learning trajectories of other species

Who is calling? Optimizing source identification from marmoset vocalizations with hierarchical machine learning classifiers

With their highly social nature and complex vocal communication system, marmosets are important models for comparative studies of vocal communication and, eventually, language evolution. However, our knowledge about marmoset vocalizations predominantly originates from playback studies or vocal interactions between dyads, and there is a need to move towards studying group-level communication dynamics. Efficient source identification from marmoset vocalizations is essential for this challenge, and machine learning algorithms (MLAs) can aid it. Here we built a pipeline capable of plentiful feature extraction, meaningful feature selection, and supervised classification of vocalizations of up to 18 marmosets. We optimized the classifier by building a hierarchical MLA that first learned to determine the sex of the source, narrowed down the possible source individuals based on their sex and then determined the source identity. We were able to correctly identify the source individual with high precisions (87.21%–94.42%, depending on call type, and up to 97.79% after the removal of twins from the dataset). We also examine the robustness of identification across varying sample sizes. Our pipeline is a promising tool not only for source identification from marmoset vocalizations but also for analysing vocalizations of other species