Animal cognition: the benefits of remembering

This is the author accepted manuscript. The final version is available from Elsevier via the DOI in this record.How cognitive abilities evolve through natural selection is poorly understood. Two new studies show that a good spatial memory helps birds that hide their food to survive and produce more offspring

Early-Life Stress Triggers Juvenile Zebra Finches to Switch Social Learning Strategies.

This is the final version of the article. Available from Elsevier (Cell Press) via the DOI in this record.Stress during early life can cause disease and cognitive impairment in humans and non-humans alike. However, stress and other environmental factors can also program developmental pathways. We investigate whether differential exposure to developmental stress can drive divergent social learning strategies between siblings. In many species, juveniles acquire essential foraging skills by copying others: they can copy peers (horizontal social learning), learn from their parents (vertical social learning), or learn from other adults (oblique social learning). However, whether juveniles' learning strategies are condition dependent largely remains a mystery. We found that juvenile zebra finches living in flocks socially learned novel foraging skills exclusively from adults. By experimentally manipulating developmental stress, we further show that social learning targets are phenotypically plastic. While control juveniles learned foraging skills from their parents, their siblings, exposed as nestlings to experimentally elevated stress hormone levels, learned exclusively from unrelated adults. Thus, early-life conditions triggered individuals to switch strategies from vertical to oblique social learning. This switch could arise from stress-induced differences in developmental rate, cognitive and physical state, or the use of stress as an environmental cue. Acquisition of alternative social learning strategies may impact juveniles' fit to their environment and ultimately change their developmental trajectories.We thank Ben Sheldon, Kevin Laland, Will Hoppitt, Lucy Aplin, Bram Kuijper, and Willem Frankenhuis for their constructive feedback, James Sturdy for his help scoring the videos, and Roland Stump for his help setting up the PIT/RFID system. D.R.F. was funded by grants from the NSF (NSF-IOS1250895) to Margaret Crofoot and BBSRC (BB/L006081/1) to Ben Sheldon, K.A.S. was funded by a BBSRC David Phillips Research Fellowship, and N.J.B. was funded by a Netherlands Organization for Scientific Research (NWO) Rubicon grant

Wild psychometrics: Evidence for 'general' cognitive performance in wild New Zealand robins, Petroica longipes

In human psychometric testing, individuals' scores in tests of diverse cognitive processes are positively correlated, with a ‘general intelligence’ factor (g) typically accounting for at least 40% of total variance. Individual differences in cognitive ability have been extensively studied in humans, yet they have received far less attention in nonhuman animals. In particular, the development of a test battery suitable for quantifying individual cognitive performance in birds remains in its infancy. Additionally, implementing this approach in the wild, where the ecological significance of cognition can also be explored, presents considerable logistical challenges for most species. We developed a cognitive test battery for wild New Zealand North Island robins. Our battery comprised six tasks based on established measures of avian cognitive performance: a motor task, colour and shape discrimination, reversal learning, spatial memory and inhibitory control. Robins varied greatly in their ability to solve these tasks and we found weakly positive, nonsignificant correlations between most tasks. A principal components analysis of task performances yielded two factors with eigenvalues >1. The first component extracted explained over 34% of the variance in cognitive performance and all six tasks loaded positively on this first component. We show, using randomization tests, that these results are robust. Our results thus suggest that a general cognitive factor, analogous to human g, underpins cognitive performance in wild North Island robins tested in their natural habitat.This research was funded by a Fast-Start grant from the Marsden Fund of the Royal Society of New Zealand (VUW1304) and a Rutherford Foundation New Zealand Postdoctoral Fellowship to R.C.S.This is the author accepted manuscript. The final version is available from Elsevier via http://dx.doi.org/10.1016/j.anbehav.2015.08.00

Repeatable group differences in the collective behaviour of stickleback shoals across ecological contexts.

This is the final version of the article. Available from Royal Society via the DOI in this record.Establishing how collective behaviour emerges is central to our understanding of animal societies. Previous research has highlighted how universal interaction rules shape collective behaviour, and that individual differences can drive group functioning. Groups themselves may also differ considerably in their collective behaviour, but little is known about the consistency of such group variation, especially across different ecological contexts that may alter individuals' behavioural responses. Here, we test if randomly composed groups of sticklebacks differ consistently from one another in both their structure and movement dynamics across an open environment, an environment with food, and an environment with food and shelter. Based on high-resolution tracking data of the free-swimming shoals, we found large context-associated changes in the average behaviour of the groups. But despite these changes and limited social familiarity among group members, substantial and predictable behavioural differences between the groups persisted both within and across the different contexts (group-level repeatability): some groups moved consistently faster, more cohesively, showed stronger alignment and/or clearer leadership than other groups. These results suggest that among-group heterogeneity could be a widespread feature in animal societies. Future work that considers group-level variation in collective behaviour may help understand the selective pressures that shape how animal collectives form and function.This research was supported by the Biotechnology and Biological Sciences Research Council (a BBSRC Graduate Research Studentship to J.W.J.), the Association for the Study of Animal Behaviour (ASAB Research Grants to J.W.J. and N.J.B.), the Royal Society (Dorothy Hodgkin Fellowship to N.J.B.) and the Deutsche Forschungsgemeinschaft (Eigene Stelle grant to K.L.L.)

Herring gulls respond to human gaze direction

This is the final version. Available from The Royal Society via the DOI in this record. Human-wildlife conflict is one of the greatest threats to species populations worldwide. One species facing national declines in the UK is the herring gull (Larus argentatus), despite an increase in numbers in urban areas. Gulls in urban areas are often considered a nuisance owing to behaviours such as food-snatching. Whether urban gull feeding behaviour is influenced by human behavioural cues, such as gaze direction, remains unknown. We therefore measured the approach times of herring gulls to a food source placed in close proximity to an experimenter who either looked directly at the gull or looked away. We found that only 26% of targeted gulls would touch the food, suggesting that food-snatching is likely to be conducted by a minority of individuals. When gulls did touch the food, they took significantly longer to approach when the experimenter's gaze was directed towards them compared with directed away. However, inter-individual behaviour varied greatly, with some gulls approaching similarly quickly in both treatments, while others approached much more slowly when the experimenter was looking at them. These results indicate that reducing human-herring gull conflict may be possible through small changes in human behaviour, but will require consideration of behavioural differences between individual gulls.Royal Society Dorothy Hodgkin Research fellowshi

The nature and nurturing of animal minds

This is the author accepted manuscript. The final version is available from Wiley via the link in this recordIntroduction:This chapter deals with ideas as old as Western philosophy itself. What is the nature of the mind, and how is it shaped? What is humanity’s place in nature? In Aristotelian philosophy, nature was conceived as a linear, ladder-like progression of forms, from the lowly to the divine. During the Middle Ages, beautiful tableaus depicted this scala naturae as a glorious ladder of life with God and heavenly beings followed in descending order down the rungs by noblemen (not women) and commoners and then in turn by wild animals, domesticated animals, plants and minerals (Figure 1). Under this view, the human mind was uniquely endowed with the capacity for thought; a capacity that separates us from the rest of the animal kingdom and links us to the divine. Whereas animals were mere automata, Descartes (1637/1994) taught that humanity had a dual nature: a material body inhabited by a divine soul (residing in the pineal gland). Through this duality, we alone could reason and think. [...

Effects of food type and abundance on begging and sharing in Asian small-clawed otters (Aonyx cinereus)

This is the final version. Available from PeerJ via the DOI in this record. The following information was supplied regarding data availability: Data and code are available at Figshare: https://figshare.com/authors/Madison_BowdenParry/9424769. Bowden-Parry, Madison; Postma, Erik; J. Boogert, Neeltje (2020): Bowden-ParryOtterdata.csv. figshare. Dataset. https://doi.org/10.6084/m9.figshare. 13017158.v2 Bowden-Parry, Madison; Postma, Erik; J. Boogert, Neeltje (2020): Bowden-ParryOtterRScript.R. figshare. Software. https://doi.org/10.6084/m9.figshare. 13016888.v2 Bowden-Parry, Madison; Postma, Erik; J. Boogert, Neeltje (2020): Bowden-ParryOtterDyadShare.csv. figshare. Dataset. https://doi.org/10.6084/m9.figshare. 13017137.v1.Begging for food, a conspicuous solicitation display, is common in a variety of taxa, and it has received extensive research attention in a parent-offspring context. Both theoretical models and empirical evidence suggest that offspring begging can be an honest signal of hunger or a mediator of competition between siblings. At a behavioural mechanistic level, begging for food can be a form of harassment aimed at persuading those in possession of food to share. Food sharing, defined as the transfer of a defendable food item from one individual to another, can vary considerably between species, age-classes and food type and abundance. We investigated the determinants of begging and food-sharing behaviours in Asian small-clawed otters (Aonyx cinereus), a group-living species that commonly exhibits begging in captivity. We presented two captive otter populations with three food types that varied in exploitation complexity, in three different abundances. We predicted that begging rates would be highest when food was in lowest abundance and hardest to exploit, and that increased begging would lead to increased food sharing. We found that, over time, increased begging rates were indeed correlated with increased food transfers, but neither food type complexity nor abundance affected begging or sharing rates. However, age category was significantly associated with begging and food sharing rates: juvenile otters begged more and shared less than adult otters. The results from this first experimental study on begging and food sharing within the Mustelid family begin to reveal some of the drivers of these behaviours

The role of animal cognition in human-wildlife interactions

This is the final version. Available on open access from Frontiers Media via the DOI in this record. Humans have a profound effect on the planet’s ecosystems, and unprecedented rates of human population growth and urbanization have brought wild animals into increasing contact with people. For many species, appropriate responses toward humans are likely to be critical to survival and reproductive success. Although numerous studies have investigated the impacts of human activity on biodiversity and species distributions, relatively few have examined the effects of humans on the behavioral responses of animals during human-wildlife encounters, and the cognitive processes underpinning those responses. Furthermore, while humans often present a significant threat to animals, the presence or behavior of people may be also associated with benefits, such as food rewards. In scenarios where humans vary in their behavior, wild animals would be expected to benefit from the ability to discriminate between dangerous, neutral and rewarding people. Additionally, individual differences in cognitive and behavioral phenotypes and past experiences with humans may affect animals’ ability to exploit human-dominated environments and respond appropriately to human cues. In this review, we examine the cues that wild animals use to modulate their behavioral responses toward humans, such as human facial features and gaze direction. We discuss when wild animals are expected to attend to certain cues, how information is used, and the cognitive mechanisms involved. We consider how the cognitive abilities of wild animals are likely to be under selection by humans and therefore influence population and community composition. We conclude by highlighting the need for long-term studies on free-living, wild animals to fully understand the causes and ecological consequences of variation in responses to human cues. The effects of humans on wildlife behavior are likely to be substantial, and a detailed understanding of these effects is key to implementing effective conservation strategies and managing human-wildlife conflict.Biotechnology & Biological Sciences Research Council (BBSRC

Herring gull aversion to gaze in urban and rural human settlements

This is the author accepted manuscript. The final version is available from Elsevier via the DOI in this recordWith an increasing human population and expansion of urban settlements, wild animals are often exposed to humans. As humans may be a threat, a neutral presence, or a source of food, animals will benefit from continuously assessing the potential risk posed by humans in order to respond appropriately. Herring gulls (Larus argentatus) are increasingly breeding and foraging in urban areas, and thus have many opportunities to interact with humans. We recently found that herring gulls take longer to approach food when being watched by a human. However, it is not known whether aversion to human gaze arises from experience with humans, and whether individual differences in responsiveness are a result of differential exposure. Here, we test whether herring gulls’ responses to human gaze differ according to their age class and urbanisation of their habitat. We measured the gulls’ flight initiation distance when an experimenter approached with either a direct or averted gaze. Neither gull age class nor urbanisation significantly influenced the effect of human gaze on flight initiation distance. However, as recently fledged juveniles responded strongly to the experimenter’s gaze, aversion to human gaze may not require extensive exposure to humans to develop. Gulls in urban areas could be approached more closely than those in rural areas, consistent with findings in other species. These results indicate that gaze aversion is present early in development and that exposure to humans may influence gulls’ responses to perceived risk from humans. Investigating the processes generating individual differences in responses to humans will provide further insights into human-wildlife interactions and the effects of urbanisation.Royal Societ

Consistent individual differences drive collective behaviour and group functioning of schooling fish

The ubiquity of consistent inter-individual differences in behavior (“animal personalities”) [1, 2] suggests that they might play a fundamental role in driving the movements and functioning of animal groups [3, 4], including their collective decision-making, foraging performance, and predator avoidance. Despite increasing evidence that highlights their importance [5–16], we still lack a unified mechanistic framework to explain and to predict how consistent inter-individual differences may drive collective behavior. Here we investigate how the structure, leadership, movement dynamics, and foraging performance of groups can emerge from inter-individual differences by high-resolution tracking of known behavioral types in free-swimming stickleback (Gasterosteus aculeatus) shoals. We show that individual’s propensity to stay near others, measured by a classic “sociability” assay, was negatively linked to swim speed across a range of contexts, and predicted spatial positioning and leadership within groups as well as differences in structure and movement dynamics between groups. In turn, this trait, together with individual’s exploratory tendency, measured by a classic “boldness” assay, explained individual and group foraging performance. These effects of consistent individual differences on group-level states emerged naturally from a generic model of self-organizing groups composed of individuals differing in speed and goal-orientedness. Our study provides experimental and theoretical evidence for a simple mechanism to explain the emergence of collective behavior from consistent individual differences, including variation in the structure, leadership, movement dynamics, and functional capabilities of groups, across social and ecological scales. In addition, we demonstrate individual performance is conditional on group composition, indicating how social selection may drive behavioral differentiation between individuals.We acknowledge financial support from the Biotechnology and Biological Sciences Research Council (Graduate Research Fellowship to J.W.J), the Association for the Study of Animal Behaviour (Research Grants to J.W.J and N.J.B), the Royal Society (Dorothy Hodgkin Fellowship to N.J.B), the National Science Foundation (PHY-0848755, IOS-1355061, EAGER-IOS- 1251585 to I.D.C), the Office of Naval Research (N00014-09-1-1074, N00014-14-1-0635 to I.D.C), the Army Research Office (W911NG-11-1-0385, W911NF-14-1-0431 to I.D.C), the Human Frontier Science Program (RGP0065/2012 to I.D.C), the Ministerium für Wissenschaft, Forschung und Kunst Baden- Württemberg (SI-BW to I.D.C), and the Max Planck Institute for Ornithology. Open Access funded by Biotechnology and Biological Sciences Research Counci