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ABSTRACT Neophobia, avoidance of novel stimuli, is an ecologically and evolutionarily relevant behavioural trait that varies among individuals and across species. Especially among wild animals, the neuromolecular mechanisms underlying individual variation in neophobia have not been well characterised. We examined three neophobic behaviours in captive female and male Eurasian tree sparrows (Passer montanus) from a wild population introduced to the USA in 1870: responses towards novel objects, novel foods, and repeated presentations of the same initially novel object. We compared transcriptomic patterns associated with neophobia in three brain regions, the striatum, dorsal hippocampus, and rostral hippocampus, using differential expression and co‐expression network analyses. We found that the striatum and hippocampus had distinct transcriptomic profiles, as did the rostral and caudal subregions of the hippocampus, supporting recent hypotheses that these subregions are functionally specialised. Despite the absence of sex differences in neophobic behaviours, neophobia‐associated gene modules revealed sex‐specific patterns within brain regions. For females, neophobic behaviours more strongly correlated with gene modules in the caudal hippocampus, a region involved in stress and anxiety, whereas for males, neophobic behaviours correlated with gene modules in the rostral hippocampus, a region that may play a larger role in spatial cognition. These modules exhibited significant overlap, suggesting that neophobic behaviours in both females and males are driven by shared neurobiological mechanisms, though they exhibit sex‐specific patterns of brain region localization. Further, this work highlights the importance of examining both male and female animals in neurobiological research. 

Abstract Neophobia, an aversive response to novelty, is a behavior with critical ecological and evolutionary relevance for wild populations because it directly influences animals’ ability to adapt to new environments and exploit novel resources. Neophobia has been described in a wide variety of different animal species from arachnids to zebra finches. Because of this widespread prevalence and ecological importance, the number of neophobia studies has continued to increase over time. However, many neophobia studies (as well as many animal behavior studies more generally) suffer from one or more of what we have deemed the “seven deadly sins” of neophobia experimental design. These “sins” include: (1) animals that are not habituated to the testing environment, (2) problems with novel stimulus selection, (3) non-standardized motivation, (4) pseudoreplication, (5) lack of sufficient controls, (6) fixed treatment order, and (7) using arbitrary thresholds for data analysis. We discuss each of these potential issues in turn and make recommendations for how to avoid them in future behavior research. More consistency in how neophobia studies are designed would facilitate comparisons across different populations and species and allow researchers to better understand whether neophobia can help explain animals’ responses to human-altered landscapes and the ability to survive in the Anthropocene. 

Behavioural syndromes are suites of correlated behaviours at the population or species level that can affect how wild animals respond to their environments, including potentially stressful situations such as captivity. In this study, we assessed whether beak wiping, a stereotyped anxiety-linked behaviour where birds wipe their beaks on a perch in a “windshield wiper” motion, was correlated with another anxiety-linked behaviour, neophobia to- wards novel objects presented with food, in captive house sparrows (Passer domesticus). We predicted that more neophobic sparrows would also exhibit more beak-wiping stereotypies. We analyzed 1 h long control videos (when sparrows were presented with a normal food dish only; n = 54) from three previous neophobia studies to assess beak wiping frequency, mean beak wiping bout duration, and total bout duration. Sparrows’ reluctance to feed in the presence of novel objects was significantly correlated with the mean duration of beak wiping bouts during control trials. We also found that simple enrichment (rubber perches, manzanita branch perches, and/or artificial pine branches) decreased both the frequency and duration of beak wiping. These findings suggest that high neophobia and high levels of stereotypy may arise due to similar neuroendocrine mechanisms and reflect a “high anxiety” behavioural syndrome. This work also highlights the importance of providing species-appropriate environmental enrichment to decrease the prevalence of stereotypic behaviours in captive songbirds. 

Neophobia, or aversion to novelty, is important for adaptability and survival as it influences the ways in which animals navigate risk and interact with their environments. Across individuals, species and other taxonomic levels, neophobia is known to vary considerably, but our understanding of the wider ecological drivers of neophobia is hampered by a lack of comparative multispecies studies using standardized methods. Here, we utilized the ManyBirds Project, a Big Team Science large-scale collaborative open science framework, to pool efforts and resources of 129 collaborators at 77 institutions from 24 countries worldwide across six continents. We examined both difference scores (between novel object test and control conditions) and raw data of latency to touch familiar food in the presence (test) and absence (control) of a novel object among 1,439 subjects from 136 bird species across 25 taxonomic orders incorporating lab, field, and zoo sites. We first demonstrated that consistent differences in neophobia existed among individuals, among species, and among other taxonomic levels in our dataset, rejecting the null hypothesis that neophobia is highly plastic at all taxonomic levels with no evidence for evolutionary divergence. We then tested for effects of ecological factors on neophobia, including diet, sociality, habitat, and range, while accounting for phylogeny. We found that (i) species with more specialist diets were more neophobic than those with more generalist diets, providing support for the Neophobia Threshold Hypothesis; (ii) migratory species were also more neophobic than nonmigratory species, which supports the Dangerous Niche Hypothesis. Our study shows that the evolution of avian neophobia has been shaped by ecological drivers and demonstrates the potential of Big Team Science to advance our understanding of animal behavior. 

Neophobia, aversive behaviour towards novel objects, foods and environments, is a trait that affects the ability of animals to adapt to new environments and exploit novel resources. Our previous work demonstrated that individual responses of house sparrows (Passer domesticus) to object neophobia trials were not correlated with time spent in or latency to enter a novel environment. However, because no positive stimulus was present in the novel environment, this study may have measured spatialneophilia. In the present study, we placed familiar food dishes in a novel environment and assessed whether an individual’s willingness to enter and feed was significantly correlated with its willingness to feed from a familiar dish containing a novel object in the home cage. We exposed house sparrows (n= 26) to a novel environment and measured their latency to enter and feed, total time spent in the novel environment and total feeding time. Sparrows were also assessed for object neophobia in their home cage. Results indicated that there were no correlations between any of the measured behaviours in the novel environment and individual responses to novel object trials, suggesting that even with food as a common motivator, spatial neophobia and object neophobia represent two distinct traits. 

Avoidance of novel stimuli (neophobia) affects how wild animals interact with their environment and may partly determine whether animals persist in human-altered landscapes. The neuroendocrine mediators of neophobia are poorly understood, although past work demonstrated that experimentally reducing circulating corticosterone in wild-caught house sparrows (Passer domesticus) decreased neophobia toward novel objects placed near the food dish. In this experiment, we directly tested the role of one of the two types of corticosterone receptors, the glucocorticoid receptor (GR), in mediating neophobia in house sparrows by administering a GR antagonist (RU486, n = 10) or a vehicle control (peanut oil, n = 10) over 5 consecutive days and measuring responses to novel objects both pre- and post-treatment. We also measured baseline and stress-induced corticosterone in all sparrows on the final day of behavior trials. To better understand the effects of RU486 on corticosterone over time, in a separate group of sparrows (n = 12) we administered RU486 or vehicle over 5 days and took multiple blood samples to assess baseline and stress-induced corticosterone. Overall, we did not detect an effect of subcutaneous RU486 injections on neophobia behavior. However, we did find that RU486 injections significantly decreased stress-induced corticosterone levels starting 1 day post-injection and baseline corticosterone levels starting 6 days post-injection, compared to vehicle-injected controls. Our results suggest that GR is not involved in mediating neophobia behavior in house sparrows. 

Some individuals respond to new objects, foods, or environments with wariness (neophobia), whereas others are willing to approach and explore. Because novel stimuli can represent both dangers and resources, group-living species may show adaptive plasticity in neophobia in response to social cues. To better understand how conspecific calls can influence neophobia in a highly gregarious species, we exposed individual house sparrows (Passer domesticus) to either conspecific alarm calls (n = 12), conspecific contact calls (n = 12), or no playback (n = 12) and measured latency to feed in the presence of novel objects. We also measured novelty responses with no sound the week before and after the sound treatment week for all individuals. Relative to no playback and contact calls, we predicted that conspecific alarm calls would increase neophobia behavior during the acoustic trial and that these effects would persist the week after exposure. Instead, we found that individuals in the contact call and no playback groups became less neophobic as weeks progressed, while the alarm call group showed no attenuation of neophobia. There was a significant interaction between week and treatment, where neophobia responses over the three weeks were significantly different for individuals exposed to alarm calls compared to the contact and no playback groups combined. These results suggest that house sparrows learn social information about potentially threatening stimuli from conspecific alarm calls; here, that novel objects may be dangerous.