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

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          Abstract

          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.

          Supplementary Information

          The online version contains supplementary material available at 10.1186/s12983-021-00417-w.

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          Most cited references61

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          Fission‐Fusion Dynamics

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            Fission-fusion dynamics, behavioral flexibility, and inhibitory control in primates.

            The Machiavellian Intelligence or Social Brain Hypothesis explains the evolution of increased brain size as mainly driven by living in complex organized social systems in which individuals represent "moving targets" who can adopt multiple strategies to respond to one another. Frequently splitting and merging in subgroups of variable composition (fission-fusion or FF dynamics) has been proposed as one aspect of social complexity ( compare with) that may be associated with an enhancement of cognitive skills like inhibition, which allows the suppression of prepotent but ineffective responses in a changing social environment. We compared the performance of primates experiencing high levels of FF dynamics (chimpanzees, bonobos, orangutans, and spider monkeys) to that of species living in more cohesive groups (gorillas, capuchin monkeys, and long-tailed macaques) on five inhibition tasks. Testing species differing in diet, phylogenetic relatedness, and levels of FF dynamics allowed us to contrast ecological, phylogenetic, and socioecological explanations for interspecific differences. Spider monkeys performed at levels comparable to chimpanzees, bonobos, and orangutans, and better than gorillas. A two-cluster analysis grouped all species with higher levels of FF dynamics together. These findings confirmed that enhanced inhibitory skills are positively associated with FF dynamics, more than to phylogenetic relations or feeding ecology.
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              The social brain hypothesis and its implications for social evolution.

              R. Dunbar (2016)
              The social brain hypothesis was proposed as an explanation for the fact that primates have unusually large brains for body size compared to all other vertebrates: Primates evolved large brains to manage their unusually complex social systems. Although this proposal has been generalized to all vertebrate taxa as an explanation for brain evolution, recent analyses suggest that the social brain hypothesis takes a very different form in other mammals and birds than it does in anthropoid primates. In primates, there is a quantitative relationship between brain size and social group size (group size is a monotonic function of brain size), presumably because the cognitive demands of sociality place a constraint on the number of individuals that can be maintained in a coherent group. In other mammals and birds, the relationship is a qualitative one: Large brains are associated with categorical differences in mating system, with species that have pairbonded mating systems having the largest brains. It seems that anthropoid primates may have generalized the bonding processes that characterize monogamous pairbonds to other non-reproductive relationships ('friendships'), thereby giving rise to the quantitative relationship between group size and brain size that we find in this taxon. This raises issues about why bonded relationships are cognitively so demanding (and, indeed, raises questions about what a bonded relationship actually is), and when and why primates undertook this change in social style.
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                Author and article information

                Contributors
                alocaico@gmail.com
                Journal
                Front Zool
                Front Zool
                Frontiers in Zoology
                BioMed Central (London )
                1742-9994
                22 June 2021
                22 June 2021
                2021
                : 18
                : 30
                Affiliations
                [1 ]GRID grid.5841.8, ISNI 0000 0004 1937 0247, Department of Clinical Psychology and Psychobiology, Faculty of Psychology, , University of Barcelona, ; Barcelona, Spain
                [2 ]GRID grid.5841.8, ISNI 0000 0004 1937 0247, Institute of Neurosciences, , University of Barcelona, ; Barcelona, Spain
                [3 ]GRID grid.9647.c, ISNI 0000 0004 7669 9786, Behavioral Ecology Research Group, Institute of Biology, , University of Leipzig, ; Leipzig, Germany
                [4 ]GRID grid.419518.0, ISNI 0000 0001 2159 1813, Research Group Primate Behavioural Ecology, Department of Human Behavior, Ecology and Culture, , Max Planck Institute for Evolutionary Anthropology, ; Leipzig, Germany
                [5 ]Barcelona Zoo, Barcelona, Spain
                Author information
                http://orcid.org/0000-0001-8836-3313
                Article
                417
                10.1186/s12983-021-00417-w
                8218502
                33397385
                9c1b2d4c-21bf-46e6-9867-30a16883ffb3
                © The Author(s) 2021

                Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

                History
                : 7 May 2020
                : 10 April 2021
                Funding
                Funded by: Zoo of Barcelona
                Award ID: PRIC grant, 2016/2017
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2021

                Animal science & Zoology
                ungulate,object permanence,acoustic cues,cognition,bovids,bison,buffalo,giraffe,test battery,memory

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