Hunt or hide: How insularity and urbanization affect foraging decisions in lizards

Foraging decisions should reflect a balance between costs and benefits of alternative strategies. Predation risk and resource availability in the environment may be crucial in deciding how cautious individuals should behave during foraging. These costs and benefits will vary in time and context, meaning that animals should be able to adjust their foraging behaviour to new or altered environments. Studying how animals do this is essential to understand their survival in these environments. In this study, we investigated the effect of both insularity and urbanization on risk‐taking and neophobia during foraging in the Dalmatian wall lizard (Podarcis melisellensis). Small islets tend to have both a lower number of predators and less resources. Therefore, islet populations were expected to show more risk‐taking behaviour and less neophobia in a foraging context. Previous studies on behaviour of urban lizards have yielded inconsistent results, but due to a lack of both predators and arthropod prey in urban habitats, we expected urban lizards to also take more risks and behave less neophobic. We sampled several inhabited and uninhabited locations on Vis (Croatia) and surrounding islets. Risk‐taking behaviour was tested by measuring the latency of lizards to feed in the presence of a predator model, and neophobia by measuring the latency to feed in the presence of a novel object. We found that islet lizards do indeed take more risks and were less vigilant, but not less neophobic. Urban and rural lizards did not differ in any of these behaviours, which is in sharp contrast with previous work on mammals and birds. The behavioural differences between islet and island lizards were novel, but not unexpected findings and are in line with the theory of “island tameness”. The effect of urbanization on the behaviour of animals seems to be more complex and might vary among taxa.     

Explaining the Paradox of Neophobic Explorers: The Social Information Hypothesis

How animals react to novel food and objects is commonly thought of as a crucial step toward innovations. One would therefore expect innovative species to be attracted to novelty and benefit from a combination of low neophobia and a high motivation to explore. Here we draw attention to the innovation paradox: the most innovative species tend to show neophobic reactions when confronted with novel objects or food, but can use social cues to overcome their initial neophobia. Work on novelty response has highlighted the role of ecological factors as determinants of neophobia and exploration tendency. We examine social influences on novelty response and present the idea that social factors enable some species to maintain the paradoxical combination of high neophobia and high exploration tendency. We compare primates with other species, to assess the extent to which primates are unusual. We review empirical studies that show how intrinsic neophobia is generally overcome by social facilitation and social information, i.e., the presence of experts, especially in species with slow life history, probably because social information reduces risk. We also briefly discuss the role of environmental risk in reducing intrinsic neophobia, in particular its absence in captivity. We draw attention to a strong neophobia-reducing effect of being in captivity, due to humans acting as sources of social information. We propose that species showing the paradoxical combination of strong neophobia and strong exploration tendency use social information to select aspects of the environment worth exploring. The social information hypothesis thus offers an explanation for the paradox of neophobic explorers.     

Effects of Group Size on Approach to Novel Objects in Ravens (Corvus corax)

Neophobia may constrain explorative behaviour, learning and innovation, while social context may facilitate approach to novel objects and acceptance of novel food. We examined the effects of neophobia on the exploration of novel objects in relation to social context in ravens (Corvus corax). Ravens are suitable subjects for studying effects of social context, as they are highly neophobic scavengers that recruit conspecifics to food. We tested two groups of six and 11 hand‐raised birds in three conditions: single‐bird, in dyadic combinations and sibling sub‐groups of three to six birds. Contrary to expectation, individuals of both groups were quicker to approach novel objects when tested alone than when tested with conspecifics. However, they spent more time close to and manipulating the novel objects in the social conditions (dyadic and group) than when being alone. We discuss the possibility that the higher latencies of dyads and groups to approach novel objects may reflect a ‘negotiation’ process in a ‘war of attrition’ between the individuals over risk‐taking.     

Urbanization and its effects on personality traits: a result of microevolution or phenotypic plasticity?

Human‐altered environmental conditions affect many species at the global scale. An extreme form of anthropogenic alteration is the existence and rapid increase of urban areas. A key question, then, is how species cope with urbanization. It has been suggested that rural and urban conspecifics show differences in behaviour and personality. However, (i) a generalization of this phenomenon has never been made; and (ii) it is still unclear whether differences in personality traits between rural and urban conspecifics are the result of phenotypic plasticity or of intrinsic differences. In a literature review, we show that behavioural differences between rural and urban conspecifics are common and taxonomically widespread among animals, suggesting a significant ecological impact of urbanization on animal behaviour. In order to gain insight into the mechanisms leading to behavioural differences in urban individuals, we hand‐raised and kept European blackbirds (Turdus merula) from a rural and a nearby urban area under common‐garden conditions. Using these birds, we investigated individual variation in two behavioural responses to the presence of novel objects: approach to an object in a familiar area (here defined as neophilia), and avoidance of an object in a familiar foraging context (defined as neophobia). Neophilic and neophobic behaviours were mildly correlated and repeatable even across a time period of one year, indicating stable individual behavioural strategies. Blackbirds from the urban population were more neophobic and seasonally less neophilic than blackbirds from the nearby rural area. These intrinsic differences in personality traits are likely the result of microevolutionary changes, although we cannot fully exclude early developmental influences.     

Rhesus macaques (Macaca mulatta) are not neophobic toward novel food with a high sugar content

While we know that food neophobia in nonhuman primates is affected by social factors, little is known about how palatability, and specifically sugar content, might ameliorate a monkey's hesitancy to eat a novel food. It is likely that an innate preference for sweet substances would alter an animal's typical neophobic response. To test this, I presented nine male rhesus macaques with novel foods that contained a low, high, or no amount of sugar. As expected, the monkeys exhibited a neophobic response to the no-sugar novel foods but not to the high-sugar novel foods. Previous research on food neophobia may need to be reevaluated in light of the effects of sugar content on the neophobic response.     

Dominance and neophobia in coyote (Canis latrans) breeding pairs

Previous research suggests that within social animals, subordinate individuals are less neophobic than dominant individuals. We investigated the effect of social status on neophobic responses using 10 captive coyote breeding pairs. Social status was determined from observations of feeding behavior and agonistic interactions during a series of reference trials. Once dominance was established, we surrounded an experimental area with novel stimuli (ropes adorned with interspersed flags) to create a novel context around a familiar food source. Contrary to hypotheses, dominant coyotes were first to feed, showed more interest toward novel stimuli, and eventually crossed the barrier, which subordinates never did. Our results indicate that dominant coyotes are less neophobic of novel settings that contain familiar food than subordinates are. Since a reduction in neophobia can be interpreted as an increase in risk taking, our results support previous observations that dominant (alpha) coyotes take more risks than subordinates. Our results also suggest reasons for differential observations of coyote behavior in the field: artificial selection against bold behavior in populations undergoing predator control.     

Do neophobia and dietary wariness explain ecological flexibility? An analysis with two seed‐eating birds of contrasting habits

The neophobia threshold hypothesis (NTH) suggests that the acquisition and maintenance of a high behavioral and ecological flexibility in the evolutionary and adaptive history of a species is the consequence of lower levels of neophobia towards new micro‐habitats and of dietary wariness of novel foods. To test this idea we assessed the degree of neophobia and dietary wariness in two seed‐eating bird species with contrasting degrees of ecological flexibility that inhabit the central Monte desert (Argentina): a grass‐seed specialist, the many‐colored chaco‐finch, and a generalist feeder, the rufous‐collared sparrow. We expected that both species would exhibit neophobia and wariness when faced with new foraging opportunities but that the rufous‐collared sparrow would be less neophobic and less wary than the specialized many‐colored chaco‐finch. Experimental indicators of neophobia and dietary wariness included willingness to eat near novel objects and willingness to eat novel seeds, respectively. Both species showed similar levels of reluctance to novelty, although the sparrow could be slightly more reluctant than the finch. Contrary to our predictions, the sparrow was neither less hesitant nor faster or greedier than the finch. This experimental evidence does not support a negative relationship between neophobia/wariness and ecological flexibility in these two seed‐eating birds and it coincides with the growing evidence that challenges the NTH. Some of our results provide support for the dangerous niche hypothesis, especially as the rufous‐collared sparrow, that feeds on more diverse and potentially dangerous food, showed higher levels of neophobia in some cases. Although the idea of neophobia and wariness being plausible causes of ecological specialization sounds attractive, the current situation calls for further research so that the causes of ecological flexibility in granivorous birds can be better understood.     

Individual and Sex Differences in Habituation and Neophobia in House Sparrows (Passer domesticus)

Heterogeneity in the environment favours foragers that are flexible (phenotypically plastic). However, consistent individual differences in behaviour (personality), such as in risk‐taking, might affect an individual's ability to find food, avoid predators and adjust to new conditions. It is now well known that personalities exist in many taxa, but much less is known about individual variation in plasticity. We measured the tendency to begin foraging across different levels of risk in house sparrows (Passer domesticus), using a behavioural reaction norm framework to simultaneously assess personality and plasticity. We asked whether individuals were consistently different across risk levels, and whether they differed in habituation and neophobia, both of which were treated as cases of plasticity. We found that males habituated more than females by beginning to feed sooner after repeated instances of a human disturbance in the presence of an initially unfamiliar object. Individuals of both sexes also exhibited consistent differences across trials, but did not differ in the rate of habituation beyond the difference between the sexes. When a novel object was placed in the foraging area, both sexes exhibited similar degrees of neophobia by delaying feeding. The magnitude of this change varied among birds, indicating individual differences in neophobia. Our results indicate that both personality and individual variation in plasticity exist but should be treated as independent phenomena. The presence of variation in plasticity implies that the raw material necessary for selection on neophobia exists, and that if heritable, plasticity in risk‐taking across contexts could evolve.     

Predator-induced neophobia in juvenile cichlids

Predation is an important but often fluctuating selection factor for prey animals. Accordingly, individuals plastically adopt antipredator strategies in response to current predation risk. Recently, it was proposed that predation risk also plastically induces neophobia (an antipredator response towards novel cues). Previous studies, however, do not allow a differentiation between general neophobia and sensory channel-specific neophobic responses. Therefore, we tested the neophobia hypothesis focusing on adjustment in shoaling behavior in response to a novel cue addressing a different sensory channel than the one from which predation risk was initially perceived. From hatching onwards, juveniles of the cichlid Pelvicachromis taeniatus were exposed to different chemical cues in a split-clutch design: conspecific alarm cues which signal predation risk and heterospecific alarm cues or distilled water as controls. At 2 months of age, their shoaling behavior was examined prior and subsequent to a tactical disturbance cue. We found that fish previously exposed to predation risk formed more compact shoals relative to the control groups in response to the novel disturbance cue. Moreover, the relationship between shoal density and shoal homogeneity was also affected by experienced predation risk. Our findings indicate predator-induced, increased cross-sensory sensitivity towards novel cues making neophobia an effective antipredator mechanism.     

Novelty Responses in a Bird Assemblage Inhabiting an Urban Area

Neophobia, or the hesitancy to approach a novel food item, object, or place, is an important factor influencing the foraging behavior of animals. Environmental factors (e.g. rapid anthropogenic changes, migration into new habitats) are associated with novelty in feeding ecology and may affect neophobic responses. Mechanisms that underlie the differential neophobic response may involve complex interactions with the environment: post-fledging experience in a greater diversity of habitats or in habitats that are more complex may contribute to reduced neophobia. In a previous study, it was observed that some urbanized species, in particular house sparrows ( Passer domesticus ) and shiny cowbirds ( Molothrus bonariensis ) show high levels of neophobia. This study was carried out in a suburban marsh of Cortaderia selloana , a relatively simple and predictable ecosystem as compared to urban areas. For this reason, in the present study, we explored novelty responses of bird species inhabiting an urban area, representing a complex environment. The results were compared to those obtained previously in the suburban marsh. We found unexpectedly high levels of neophobia in house sparrows, but shiny cowbirds showed a somewhat neophilic response. In the presence of novel objects, house sparrows tended to enter the feeders alone, while shiny cowbirds tended to forage in groups. We found no differences in latencies to forage or in visit duration between habitat types, but the proportion of individuals that visited the feeders when novel objects were present was lower in the urban area for house sparrows and eared doves ( Zenaida auriculata ). The results are discussed in the context of invasion success and feeding innovation in shiny cowbirds.     

Habitat degradation disrupts neophobia in juvenile coral reef fish

Habitat degradation not only disrupts habitat‐forming species, but alters the sensory landscape within which most species must balance behavioural activities against predation risk. Rapidly developing a cautious behavioural phenotype, a condition known as neophobia, is advantageous when entering a novel risky habitat. Many aquatic organisms rely on damage‐released conspecific cues (i.e. alarm cues) as an indicator of impending danger and use them to assess general risk and develop neophobia. This study tested whether settlement‐stage damselfish associated with degraded coral reef habitats were able to use alarm cues as an indicator of risk and, in turn, develop a neophobic response at the end of their larval phase. Our results indicate that fish in live coral habitats that were exposed to alarm cues developed neophobia, and, in situ, were found to be more cautious, more closely associated with their coral shelters and survived four‐times better than non‐neophobic control fish. In contrast, fish that settled onto degraded coral habitats did not exhibit neophobia and consequently suffered much greater mortality on the reef, regardless of their history of exposure to alarm cues. Our results show that habitat degradation alters the efficacy of alarm cues with phenotypic and survival consequences for newly settled recruits.     

Cautious Crows: Neophobia in Torresian Crows (Corvus orru) Compared with Three Other Corvoids in Suburban Australia

Corvids (Family: CORVIDAE) are a clade of some 120 species widespread throughout much of the world that have attracted the interest of researchers due to their impressive cognitive abilities. The group is, however, also generally described as neophobic, a trait that increases the difficulty of undertaking such research. In Australia, Torresian crows (Corvus orru) have, like corvid species worldwide, thrived in urban environments, sharing this habitat with a number of other corvoid (Superfamily: CORVOIDEA) species. While each of these species has successfully colonised urban areas, the extent to which neophobia is present is not known. This study empirically tested the extent to which neophobia is exhibited in wild urban Torresian crows by measuring the delaying effect of a novel object to obtaining food and any changes in neophobic behaviours displayed. This was then compared with the other urban corvoid species that inhabit similar niches. This study confirmed that Torresian crows are significantly wary of a novel objects, displaying more neophobic behaviours and taking longer to attain the food. Crow behaviour provided evidence in support of both the dangerous niche hypothesis and the two‐factor model of neophobia and neophilia. Crows also displayed these behaviours to a significantly greater extent than the three other corvoids studied. However, the individual variation in crow behaviours when exposed to a novel object was extensive. This variation may be attributed to differing behavioural types between individuals, or different experiences with novel objects or humans in the bird's past.     

Sex‐Specific Associations Between Nest Defence,Exploration and Breathing Rate in Breeding Pied Flycatchers

Correlations between behavioural traits constrain animals to a limited range of behavioural choices and set a limit to the available variation in behavioural phenotype of a population. These constraints are especially important during stressful situations, potentially limiting the ability to cope with stress appropriately. As yet, very little consideration has been given to a possible role for sexual selection in maintaining differences in behavioural stability within individuals: sex‐specific differences in behavioural correlations have been seldom studied, especially in the wild. In this field study, we investigated associations between neophobia (latency to enter nest in the presence of a novel object), nest defence (response to a model predator) and breathing rate in response to handling in breeding pied flycatchers (Ficedula hypoleuca). We did not find any significant difference in antipredator responses between males and females, which indicates low sexual conflict over parental care in the pied flycatcher. However, females were more neophobic than males, while males and females did not differ in their breathing rates. Further, our study demonstrated a strong positive correlation between nest defence behaviour and neophobia in male, but not in female pied flycatchers. Males that defended their nest more had lower breathing rate and higher latency to resume nestling feeding after encountering a predator decoy than males that mobbed less intensely. We found only weak evidence that nest partners might affect each other's behaviour in these contexts.     

Social learning in a high-risk environment: incomplete disregard for the ‘minnow that cried pike’ results in culturally transmitted neophobia

Many prey species rely on conspecifics to gather information about unknown predation threats, but little is known about the role of varying environmental conditions on the efficacy of social learning. We examined predator-naive minnows that had the opportunity to learn about predators from experienced models that were raised in either a low- or high-risk environment. There were striking differences in behaviour among models; high-risk models showed a weaker response to the predator cue and became neophobic in response to the control cue (a novel odour, NO). Observers that were previously paired with low-risk models acquired a strong antipredator response only to the predator cue. However, observers that interacted with high-risk models, displayed a much weaker response to the predator odour and a weak neophobic response to the NO. This is the first study reporting such different outcomes of social learning under different environmental conditions, and suggests high-risk environments promote the cultural transmission of neophobia more so than social learning. If such a transfer can be considered similar to secondary traumatization in humans, culturally transmitted neophobia in minnows may provide a good model system for understanding more about the social ecology of fear disorders.     

Head Colour and Age Relate to Personality Traits in Gouldian Finches

Colour polymorphism is a widespread phenomenon in vertebrates and has often been linked with differences in behaviour such as aggression or boldness, behaviours that are often part of personality traits in monomorphic species. However, up to now, very few studies have looked whether colour morphs just differ in average behaviour or whether specific combinations of behaviours are favoured in relation to a particular morph therefore signalling personality traits. This was tested in the highly social and polymorphic Gouldian finch (Erythrura gouldiae). Tests were performed in pairs of a red‐headed and a black‐headed individual of same sex and size but different age. Capture rank in the aviary as well as latency to feed beside a novel object (neophobia) and to approach and touch a novel object on a perch (neophilia) were measured. For neophobia and neophilia, ranks of latencies calculated across all individuals were used and general and within‐pair comparisons were made. Neophobia and approach neophilia were consistent over time (2 mo), and approach neophilia was positively correlated with capture rank and neophobia indicating that the behaviours are part of personality traits. Moreover, black‐headed birds generally approached the novel object earlier than red‐headed birds. Similarly, within pairs, black‐headed birds were first to approach the novel object and were also captured first. Relative age (younger or older than the partner) was related to neophobia and tactile neophilia ranks; older birds reacted faster. The results indicate that colour morphs not only differ in average behaviour but that specific combinations of behaviours are related to colour morphs suggesting that head colours signal personality traits. Furthermore, depending on age individuals may have different roles in a social network.     

Species specific behavioural patterns (digging and swimming) and reaction to novel objects in wild type, Wistar, Sprague-Dawley and Brown Norway rats

Background

The purpose of the present study was to analyse species-specific forms of behaviour (digging and swimming) and response to novelty in laboratory rats and their wild type counterparts at a very early stage of laboratorization. Three behavioural phenomena were taken into account: burrowing, spontaneous swimming, and neophobic behaviour.

Principal Findings

Wild-type rats and three strains of laboratory rats were involved in experiments: Warsaw-Wild-Captive-Pisula-Stryjek (WWCPS), Wistar, Sprague-Dawley, and Brown Norway rats were compared in spontaneous swimming test, while WWCPS and Wistar rats were studied in burrowing and neophobia experiments. Wild rats were found to be faster at building tunnels than Wistar rats and at constructing more complex burrow systems. The experiment on neophobia showed that Wistar rats exhibited less neophobic responses and were more often trapped. WWCPS rats showed highly neophobic behaviour and were rarely trapped in this experiment. The experiment on swimming showed that WWCPS rats showed more complex water tank related activity than their laboratory counterparts. They swam and explored under surface environment.

Conclusions

The three experiments showed profound behavioural differences in quasi-natural forms of behaviour between wild type rats (WWCPS) and three laboratory strains frequently used in behavioural studies.     

Integrating sensory ecology and predator-prey theory to understand animal responses to fire

Fire regimes are changing dramatically worldwide due to climate change, habitat conversion, and the suppression of Indigenous landscape management. Although there has been extensive work on plant responses to fire, including their adaptations to withstand fire and long-term effects of fire on plant communities, less is known about animal responses to fire. Ecologists lack a conceptual framework for understanding behavioural responses to fire, which can hinder wildlife conservation and management. Here, we integrate cue-response sensory ecology and predator-prey theory to predict and explain variation in if, when and how animals react to approaching fire. Inspired by the literature on prey responses to predation risk, this framework considers both fire-naïve and fire-adapted animals and follows three key steps: vigilance, cue detection and response. We draw from theory on vigilance tradeoffs, signal detection, speed-accuracy tradeoffs, fear generalization, neophobia and adaptive dispersal. We discuss how evolutionary history with fire, but also other selective pressures, such as predation risk, should influence animal behavioural responses to fire. We conclude by providing guidance for empiricists and outlining potential conservation applications.     

Androgens Increase Persistence But Do Not Affect Neophobia in a Problem‐Solving Context in a Songbird

Gonadal steroid hormones enhance cognitive performance, particularly spatial and vocal learning, in mammals and birds. However, it is unknown whether problem‐solving ability is similarly regulated. We propose that androgens, such as testosterone and 5α‐dihydrotestosterone, play a role in mediating problem‐solving behavior as well. As a test, male white‐crowned sparrows (Zonotrichia leucophrys gambelii) were either castrated and administered a blank (Blank‐castrate) or testosterone‐filled implant (T‐castrate) or were sham operated and were exposed to a novel feeder, which they had to open to receive a food reward, in two trials. Testosterone treatment affected neither a neophobic response nor problem‐solving performance. However, T‐castrates were more persistent in manipulating the feeder than Blank‐castrates or Shams. Furthermore, their persistence correlated positively with circulating levels of both testosterone and 5α‐dihydrotestosterone. We suggest that a positive correlation between sex steroids and persistence in foraging and problem‐solving contexts may lead to an adaptive increase in resource acquisition in the breeding season. Given the overall low success on the problem‐solving test, we cannot confidently conclude that androgens do not play a role in mediating problem‐solving behavior. However, unlike in mammals, it seems these hormones do not significantly influence neophobia in foraging contexts in birds.     

Neophobia and its effect on the macro-structure and micro-structure of feeding in wild brown rats (Rattus norvegicus)

The effect of neophobia (fear of novelty) on feeding behaviour was examined in two groups of captive wild rats fed ad libitum. Different individuals employed different feeding patterns in response to novelty despite the absence of social and ecological constraints. The prevalent feeding pattern was to delay eating from a novel bowl several nights after it was introduced and, in general, novel food was sampled towards the end of a night. Systematic relationships (prandial correlations) were revealed in the meal pattern data which were consistent with the prediction that post-prandial correlations (controlled regular feeding bouts) are more likely in predictable environments. A large proportion of the individuals exhibited no prandial relationships which correlated with high levels of neophobia supporting the hypothesis that highly neophobic individuals are less able to regulate their feeding in the presence of novelty.     

Yolk testosterone modulates persistence of neophobic responses in adult zebra finches, Taeniopygia guttata

Individual differences in animal behavior can be attributed to genetic as well as non-genetic influences. One mechanism by which the behavioral phenotype of an individual can be shaped is via transmission of maternal sex steroids. In this study, we examined the role of yolk testosterone (T) in controlling neophobia in 9-month-old, sexually mature zebra finches (Taeniopygia guttata). Offspring hatched from either T-treated or control eggs were subjected to a sequential series of behavioral tests in which we measured the neophobic response and its persistence towards two unfamiliar stimuli. Birds from T-treated and control eggs did not differ in their latencies to approach and eat a novel food source during their first encounter. However, egg treatment affected subsequent habituation. Latencies decreased in both groups over a habituation period of 5 days, but considerably more so in T-offspring. Although males appeared to approach novel food faster than females, there was no overall sex effect during the habituation period. When a novel object was added in combination with the previously learned food stimulus, this caused an behavioral shift in approach latencies. In males, control offspring had significantly shorter latencies than T-offspring, whereas there was no difference among females. The latency to eat in the same test was not significantly affected by sex or egg treatment. Our results demonstrate long-term effects of prenatal T on neophobic responses in adult zebra finches. We hypothesize that prenatal T may be one underlying mechanism for individual differences routine formation.