Neophobia is not only avoidance: Improving neophobia tests by combining cognition and ecology

Psychologists and behavioural ecologists use neophobia tests to measure behaviours ranging from anxiety to predatory wariness. Psychologists typically focus on underlying cognitive mechanisms at the expense of ecological validity, while behavioural ecologists generally examine adaptive function but ignore cognition. However, neophobia is an ecologically relevant fear behaviour that arises through a cognitive assessment of novel stimuli. Both fields have accrued conflicting results using various testing protocols, making it unclear what neophobia tests measure and what correlations between neophobia and other traits mean. Developing cognitively and ecologically informed tests allows neophobia to be empirically evaluated where appropriate and controlled for where it interferes with other behavioural measures. We offer guidelines for designing tests and stress the need for interdisciplinary dialogue to better explore neophobia's proximate causes and ecological consequences.We would like to thank Alecia Carter for helpful discussion and comments on the manuscript and to thank two anonymous reviewers and the editor, Dr. Hofmann, for their thoughtful and insightful feedback. A.L.G. received generous support from the Gates-Cambridge Trust; A.T. is funded by a BBSRC David Phillips Fellowship (BB/H021817/1).This is the author accepted manuscript. The final version is available from Elsevier via http://dx.doi.org/10.1016/j.cobeha.2015.10.00

Individual Variation in Dietary Wariness Is Predicted by Head Color in a Specialist Feeder, the Gouldian Finch

Shifts in resource availability due to environmental change are increasingly confronting animals with unfamiliar food types. Species that can rapidly accept new food types may be better adapted to ecological change. Intuitively, dietary generalists are expected to accept new food types when resources change, while dietary specialists would be more averse to adopting novel food. However, most studies investigating changes in dietary breadth focus on generalist species and do not delve into potential individual predictors of dietary wariness and the social factors modulating these responses. We investigated dietary wariness in the Gouldian finch, a dietary specialist, that is expected to avoid novel food. This species occurs in two main head colors (red, black), which signal personality in other contexts. We measured their initial neophobic responses (approach attempts before first feed and latency to first feed) and willingness to incorporate novel food into their diet (frequency of feeding on novel food after first feed). Birds were tested in same-sex pairs in same and different head color pairings balanced across experiments 1 and 2. Familiar and novel food (familiar food dyed) were presented simultaneously across 5 days for 3 h, each. Gouldian finches fed on the familiar food first demonstrating food neophobia, and these latencies were repeatable. Birds made more approach attempts before feeding on novel than familiar food, particularly red-headed birds in experiment 1 and when partnered with a black-headed bird. Individuals consistently differed in their rate of incorporation of novel food, with clear differences between head colors; red-headed birds increased their feeding visits to novel food across experimentation equaling their familiar food intake by day five, while black-headed birds continually favored familiar food. Results suggest consistent among individual differences in response to novel food with red-headed birds being adventurous consumers and black-headed birds dietary conservatives. The differences in food acceptance aligned with responses to novel environments on the individual level (found in an earlier study) providing individuals with an adaptive combination of novelty responses across contexts in line with potential differences in movement patterns. Taken together, these novelty responses could aid in population persistence when faced with environmental changes

Harnessing learning biases is essential for applying social learning in conservation

Social learning can influence how animals respond to anthropogenic changes in the environment, determining whether animals survive novel threats and exploit novel resources or produce maladaptive behaviour and contribute to human-wildlife conflict. Predicting where social learning will occur and manipulating its use are, therefore, important in conservation, but doing so is not straightforward. Learning is an inherently biased process that has been shaped by natural selection to prioritize important information and facilitate its efficient uptake. In this regard, social learning is no different from other learning processes because it too is shaped by perceptual filters, attentional biases and learning constraints that can differ between habitats, species, individuals and contexts. The biases that constrain social learning are not understood well enough to accurately predict whether or not social learning will occur in many situations, which limits the effective use of social learning in conservation practice. Nevertheless, we argue that by tapping into the biases that guide the social transmission of information, the conservation applications of social learning could be improved. We explore the conservation areas where social learning is highly relevant and link them to biases in the cues and contexts that shape social information use. The resulting synthesis highlights many promising areas for collaboration between the fields and stresses the importance of systematic reviews of the evidence surrounding social learning practices.BBSRC David Phillips Fellowship (BB/H021817/1

The impact of egg incubation temperature on the personality of oviparous reptiles

Personality traits, defined as differences in the behavior of individual animals of the same species that are consistent over time and context, such as ‘boldness,’ have been shown to be both heritable and be influenced by external factors, such as predation pressure. Currently, we know very little about the role that early environmental factors have upon personality. Thus, we investigated the impact of incubation temperature upon the boldness on an oviparous reptile, the bearded dragon (Pogona vitticeps). Eggs, from one clutch, were incubated at two different average temperatures within the normal range. After hatching the lizards were raised under the same environmental conditions. Novel object and novel environment tests were used to assess personality. Each test was repeated in both the short term and the long term. The results revealed that incubation temperature did impact upon ‘boldness’ but only in the short term and suggests that, rather than influencing personality, incubation temperature may have an effect on the development of behavioral of oviparous reptiles at different stages across ontogeny

Early life differences in behavioral predispositions in two Alligatoridae species

Behavioral predispositions are innate tendencies of animals to behave in a given way without the input of learning. They increase survival chances and, due to environmental and ecological challenges, may vary substantially even between closely related taxa. These diferences are likely to be especially pronounced in long-lived species like crocodilians. This order is particularly relevant for comparative cognition due to its phylogenetic proximity to birds. Here we compared early life behavioral predispositions in two Alligatoridae species. We exposed American alligator and spectacled caiman hatchlings to three different novel situations: a novel object, a novel environment that was open and a novel environment with a shelter. This was then repeated a week later. During exposure to the novel environments, alligators moved around more and explored a larger range of the arena than the caimans. When exposed to the novel object, the alligators reduced the mean distance to the novel object in the second phase, while the caimans further increased it, indicating diametrically opposite ontogenetic development in behavioral predispositions. Although all crocodilian hatchlings face comparable challenges, e.g., high predation pressure, the effectiveness of parental protection might explain the observed pattern. American alligators are apex predators capable of protecting their offspring against most dangers, whereas adult spectacled caimans are frequently predated themselves. Their distancing behavior might be related to increased predator avoidance and also explain the success of invasive spectacled caimans in the natural habitats of other crocodilians

Convergent evolution of animal intelligence

This is the author accepted manuscript.DEFINITION: When two or more distantly related species evolve similar cognitive adaptations in response to comparable environmental challenges

Wild jackdaws are wary of objects that violate expectations of animacy

This is the author accepted manuscript. The final version is available from The Royal Society via the DOI in this record.All data and R code used for the analysis of this publication can be found in the electronic supplementary material at the DOI in this record.Nature is composed of self-propelled, animate agents and inanimate objects. Laboratory studies have shown that human infants and a few species discriminate between animate and inanimate objects. This ability is assumed to have evolved to support social cognition and filial imprinting, but its ecological role for wild animals has never been examined. An alternative, functional explanation is that discriminating stimuli based on their potential for animacy helps animals distinguish between harmless and threatening stimuli. Using remote-controlled experimental stimulus presentations, we tested if wild jackdaws (Corvus monedula) respond fearfully to stimuli that violate expectations for movement. Breeding pairs (N ¼ 27) were presented at their nests with moving and non-moving models of ecologically relevant stimuli (birds, snakes and sticks) that differed in threat level and propensity for independent motion. Jackdaws were startled by movement regardless of stimulus type and produced more alarm calls when faced with animate objects. However, they delayed longest in entering their nest-box after encountering a stimulus that should not move independently, suggesting they recognized the movement as unexpected. How jackdaws develop expectations about object movement is not clear, but our results suggest that discriminating between animate and inanimate stimuli may trigger information gathering about potential threats.British Ecological Societ

Street smart: faster approach towards litter in urban areas by highly neophobic corvids and less fearful birds

ArticleThis is an open access article.The extent to which animals respond fearfully to novel stimuli may critically influence their ability to survive alongside humans. However, it is unclear whether the fear of novel objects, object neophobia, consistently varies in response to human disturbance. Where variation has been documented, it is unclear whether this variation is due to a change in fear towards specific novel stimuli, or whether it is symptomatic of a general change in fear behaviour. We measured levels of object neophobia in free-flying birds across urban and rural habitats, comparing corvids, a family known for being behaviourally flexible and innovative, with other urban-adapting bird species. Neophobic responses were measured in the presence of different types of objects that varied in their novelty, and were compared to behaviour during a baited control. Corvids were more neophobic than noncorvid species towards all object types, but their hesitancy abated after conspecifics approached in experimental conditions in which objects resembled items they may have experienced previously. Both sets of species were faster to approach objects made from human litter in urban than rural areas, potentially reflecting a category-specific reduction in fear based on experience. These results highlight species similarities in behavioural responses to human-dominated environments despite large differences in baseline neophobia.We owe a big thank you to Christopher Smith for his help in coding videos, and to Guill McIvor for his tireless ringing efforts and field support. We are very grateful to Paul Gluyas and the entire staff at Pencoose farm, to Stithians Parish Council and to David Fisher, Julian Evans and Shona Jack for allowing us to put up feeding tables on their land and in their gardens. Finally, we thank Sinéad English for advice on statistics and Laura Kelly for help with the spectral analyses. A.G. received generous support from the Gates-Cambridge Trust. A.T. was supported by a BBSRC David Phillips Fellowship (BB/H021817/1) and a grant from the British Ecological Society2769/3464

Seasonal changes in neophobia and its consistency in rooks: the effect of novelty type and dominance position

Neophobia, or the fear of novelty, may offer benefits to animals by limiting their exposure to unknown danger, but can also impose costs by preventing the exploration of potential resources. The costs and benefits of neophobia may vary throughout the year if predation pressure, resource distribution or conspecific competition changes seasonally. Despite such variation, neophobia levels are often assumed to be temporally and individually stable. Whether or not neophobia expression changes seasonally and fluctuates equally for all individuals is crucial to understanding the drivers, consequences and plasticity of novelty avoidance. We investigated seasonal differences and individual consistency in the motivation and novelty responses of a captive group of rooks, Corvus frugilegus, a seasonally breeding, colonial species of corvid that is known for being neophobic. We tested the group around novel objects and novel people to determine whether responses generalized across novelty types, and considered whether differences in dominance could influence the social risk of approaching unknown stimuli. We found that the group's level of object neophobia was stable year-round, but individuals were not consistent between seasons, despite being consistent within seasons. In contrast, the group's avoidance of novel people decreased during the breeding season, and individuals were consistent year-round. Additionally, although subordinate birds were more likely to challenge dominants during the breeding season, this social risk taking did not translate to greater novelty approach. Since seasonal variation and individual consistency varied differently towards each novelty type, responses towards novel objects and people seem to be governed by different mechanisms. Such a degree of fluctuation has consequences for other individually consistent behaviours often measured within the nonhuman personality literature.A.L.G. received generous support from the Gates-Cambridge Trust. J.W.J was supported by a BBSRC scholarship and A.T. was funded by a BBSRC David Phillips Fellowship (BB/H021817/1). Thanks also to the University of Cambridge for financial support.Open Access funded by Biotechnology and Biological Sciences Research Counci

Wild jackdaws’ reproductive success and their offspring’s stress hormones are connected to provisioning rate and brood size, not to parental neophobia

This is the author accepted manuscript. The final version is available from the publisher via the DOI in this record.Many species show individual variation in neophobia and stress hormones, but the causes and consequences of this variation in the wild are unclear. Variation in neophobia levels could affect the number of offspring animals produce, and more subtly influence the rearing environment and offspring development. Nutritional deficits during development can elevate levels of stress hormones that trigger long-term effects on learning, memory, and survival. Therefore measuring offspring stress hormone levels, such as corticosterone (CORT), helps determine if parental neophobia influences the condition and developmental trajectory of young. As a highly neophobic species, jackdaws (Corvus monedula) are excellent for exploring the potential effects of parental neophobia on developing offspring. We investigated if neophobic responses, alongside known drivers of fitness, influence nest success and offspring hormone responses in wild breeding jackdaws. Despite its consistency across the breeding season, and suggestions in the literature that it should have importance for reproductive fitness, parental neophobia did not predict nest success, provisioning rates or offspring hormone levels. Instead, sibling competition and poor parental care contributed to natural variation in stress responses. Parents with lower provisioning rates fledged fewer chicks, chicks from larger broods had elevated baseline CORT levels, and chicks with later hatching dates showed higher stress-induced CORT levels. Since CORT levels may influence the expression of adult neophobia, variation in juvenile stress responses could explain the development and maintenance of neophobic variation within the adult population.This work was supported by the Gates Cambridge Trust to ALG and two separate BBSRC David Phillips Fellowships to KAS and AT (BB/L002264/1 and BB/H021817/1)