Lab cognition going wild: Implementing a new portable touchscreen system in vervet monkeys.

Touchscreen technology has provided researchers with opportunities to conduct well-controlled cognitive tests with captive animals, allowing researchers to isolate individuals, select participants based on specific traits, and control aspects of the environment. In this study, we aimed to investigate the potential utility of touchscreen technology for the study of cognition in wild vervet monkeys. We assessed the viability of touchscreen testing by comparing rates of participation between wild and sanctuary-housed vervets. Additionally, we compared performance on a simple associative learning task in order to verify that wild participants are able to engage meaningfully with a touchscreen task presented in their natural environment. We presented eight groups of vervet monkeys (four wild and four sanctuary groups, totalling 240 individuals) with a portable touchscreen device. The touchscreen displayed tasks in which food rewards could be gained by touching a stimulus displayed on the screen. We assessed individuals' likelihood of interacting with the touchscreen, their frequency of participation, and their performance on a simple associative learning task. We found that sanctuary-housed monkeys were more likely to interact with the touchscreen. Participation in wild vervet monkeys was influenced by sex and age. However, monkeys in the two contexts (sanctuary vs. wild) did not differ in their performance on a simple associative learning task. This study demonstrates that touchscreen technology can be successfully deployed in a population of wild primates. This gives us a starting point to test animal cognition under natural conditions that include varying group composition, environmental challenges and ongoing activities such as foraging, which are challenging to recreate in captivity. While rates of participation were lower than those found in captivity, reasonable sample sizes can be achieved, and wild primates can successfully learn touchscreen tasks in a manner comparable to their captive counterparts.

[1]  T. Matsuzawa,et al.  Apex and ApeTouch: Development of a Portable Touchscreen System and Software for Primates at Zoos , 2022, Animals : an open access journal from MDPI.

[2]  Rachel A. Harrison,et al.  The unique potential of field research to understand primate social learning and cognition , 2022, Current Opinion in Behavioral Sciences.

[3]  A. Valencia-Aguilar,et al.  Wild cognition – linking form and function of cognitive abilities within a natural context , 2022, Current Opinion in Behavioral Sciences.

[4]  R. Bshary,et al.  Factors affecting tolerance persistence after grooming interactions in wild female vervet monkeys, Chlorocebus pygerythrus , 2021, Animal Behaviour.

[5]  E. A. Smeltzer,et al.  Be early or be tolerated: vervet monkey, Chlorocebus pygerythrus, foraging strategies in a dispersed resource , 2021, Animal Behaviour.

[6]  G. Cowlishaw,et al.  Individual differences in task participation in wild chacma baboons , 2021, Animal Behaviour.

[7]  C. Tennie,et al.  Chimpanzees’ (Pan troglodytes) problem-solving skills are influenced by housing facility and captive care duration , 2020, PeerJ.

[8]  Lydia M. Hopper,et al.  Within- and between-species variation in the responses of three primate species to a touchscreen gambling task , 2020 .

[9]  C. Hemelrijk,et al.  Dynamics of Intersexual Dominance and Adult Sex- Ratio in Wild Vervet Monkeys , 2020, Frontiers in Psychology.

[10]  Guidelines for the treatment of animals in behavioural research and teaching , 2020, Animal Behaviour.

[11]  R. Bshary,et al.  The past, present and future of cleaner fish cognitive performance as a function of CO2 levels , 2019, Biology Letters.

[12]  E. Waal,et al.  Primates are living links to our past: The contribution of comparative studies with wild vervet monkeys to the field of social cognition , 2019, Cortex.

[13]  Susana Carvalho,et al.  Chimpanzee face recognition from videos in the wild using deep learning , 2019, Science Advances.

[14]  Richard McFarland,et al.  Male residency and dispersal triggers in a seasonal breeder with influential females , 2019, Animal Behaviour.

[15]  Jay Wilhelm,et al.  An Arduino-Based RFID Platform for Animal Research , 2019, Front. Ecol. Evol..

[16]  K. Zuberbühler,et al.  Necessity creates opportunities for chimpanzee tool use , 2019, Behavioral Ecology.

[17]  R. Ha,et al.  Captive jays exhibit reduced problem-solving performance compared to wild conspecifics , 2019, Royal Society Open Science.

[18]  S. R. Ross,et al.  A review of zoo-based cognitive research using touchscreen interfaces. , 2018, Zoo biology.

[19]  A. Whiten,et al.  Payoff- and Sex-Biased Social Learning Interact in a Wild Primate Population , 2018, Current Biology.

[20]  A. Thornton,et al.  An intraspecific appraisal of the social intelligence hypothesis , 2018, Philosophical Transactions of the Royal Society B: Biological Sciences.

[21]  A. Whiten,et al.  Field experiments with wild primates reveal no consistent dominance-based bias in social learning , 2018, Animal Behaviour.

[22]  J. Morand‐Ferron Why learn? The adaptive value of associative learning in wild populations , 2017, Current Opinion in Behavioral Sciences.

[23]  Lydia M. Hopper Cognitive research in zoos , 2017, Current Opinion in Behavioral Sciences.

[24]  M. Whiteside,et al.  Differential participation in cognitive tests is driven by personality, sex, body condition and experience , 2017, Behavioural Processes.

[25]  Judith M Burkart,et al.  Orientation toward humans predicts cognitive performance in orang-utans , 2017, Scientific Reports.

[26]  Ella F Cole,et al.  Studying the evolutionary ecology of cognition in the wild: a review of practical and conceptual challenges , 2016, Biological reviews of the Cambridge Philosophical Society.

[27]  R. Bshary,et al.  Wild Vervet Monkeys Trade Tolerance and Specific Coalitionary Support for Grooming in Experimentally Induced Conflicts , 2015, Current Biology.

[28]  Nicole Zweifel,et al.  Contrasting responses to novelty by wild and captive orangutans , 2015, American journal of primatology.

[29]  Steven Hamblin,et al.  Taking the Operant Paradigm into the Field: Associative Learning in Wild Great Tits , 2015, PloS one.

[30]  A. Whiten,et al.  Tolerance and Social Facilitation in the Foraging Behaviour of Free-Ranging Crows (Corvus corone corone; C. c. cornix). , 2014, Ethology : formerly Zeitschrift fur Tierpsychologie.

[31]  Katherine A. Cronin,et al.  Population-level variability in the social climates of four chimpanzee societies , 2014 .

[32]  A. Whiten,et al.  Video demonstrations seed alternative problem-solving techniques in wild common marmosets , 2014, Biology Letters.

[33]  D. Bates,et al.  Fitting Linear Mixed-Effects Models Using lme4 , 2014, 1406.5823.

[34]  Sarah Benson-Amram,et al.  A comparison of innovative problem-solving abilities between wild and captive spotted hyaenas, Crocuta crocuta , 2013, Animal Behaviour.

[35]  A. Whiten,et al.  Social learning and spread of alternative means of opening an artificial fruit in four groups of vervet monkeys , 2013, Animal Behaviour.

[36]  R. Bshary,et al.  Adult Cleaner Wrasse Outperform Capuchin Monkeys, Chimpanzees and Orang-utans in a Complex Foraging Task Derived from Cleaner – Client Reef Fish Cooperation , 2012, PloS one.

[37]  A. Whiten,et al.  Spontaneous Emergence, Imitation and Spread of Alternative Foraging Techniques among Groups of Vervet Monkeys , 2012, PloS one.

[38]  A. Hinks,et al.  Cognitive Ability Influences Reproductive Life History Variation in the Wild , 2012, Current Biology.

[39]  A. Thornton,et al.  Innovative problem solving in wild meerkats , 2012, Animal Behaviour.

[40]  L. Fedigan Ethical issues faced by field primatologists: asking the relevant questions , 2010, American journal of primatology.

[41]  R. Bshary,et al.  Selective attention to philopatric models causes directed social learning in wild vervet monkeys , 2010, Proceedings of the Royal Society B: Biological Sciences.

[42]  Jennifer J. Pokorny,et al.  Monkeys recognize the faces of group mates in photographs , 2009, Proceedings of the National Academy of Sciences.

[43]  Andrew Whiten,et al.  Social facilitation of exploratory foraging behavior in capuchin monkeys (Cebus apella) , 2009, American journal of primatology.

[44]  Lars Chittka,et al.  The correlation of learning speed and natural foraging success in bumble-bees , 2008, Proceedings of the Royal Society B: Biological Sciences.

[45]  T. Matsuzawa,et al.  Working memory of numerals in chimpanzees , 2007, Current Biology.

[46]  K. Laland,et al.  Age differences in neophilia, exploration, and innovation in family groups of callitrichid monkeys , 2005, American journal of primatology.

[47]  Tetsuro Matsuzawa,et al.  Cognition: Numerical memory span in a chimpanzee , 2000, Nature.

[48]  H. Kummer,et al.  Conditions of Innovative Behaviour in Primates , 1985 .

[49]  Maria C. Tello-Ramos,et al.  Why study cognition in the wild (and how to test it)? , 2016, Journal of the experimental analysis of behavior.

[50]  T. A. Hurly,et al.  What hummingbirds can tell us about cognition in the wild , 2013 .

[51]  L. Fairbanks,et al.  Maternal protectiveness and response to the unfamiliar in vervet monkeys , 1993, American journal of primatology.