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.     

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.     

Personality traits and behavioral syndromes in differently urbanized populations of house sparrows (Passer domesticus)

Urbanization creates novel environments for wild animals where selection pressures may differ drastically from those in natural habitats. Adaptation to urban life involves changes in various traits, including behavior. Behavioral traits often vary consistently among individuals, and these so-called personality traits can be correlated with each other, forming behavioral syndromes. Despite their adaptive significance and potential to act as constraints, little is known about the role of animal personality and behavioral syndromes in animals' adaptation to urban habitats. In this study we tested whether differently urbanized habitats select for different personalities and behavioral syndromes by altering the population mean, inter-individual variability, and correlations of personality traits. We captured house sparrows (Passer domesticus) from four different populations along the gradient of urbanization and assessed their behavior in standardized test situations. We found individual consistency in neophobia, risk taking, and activity, constituting three personality axes. On the one hand, urbanization did not consistently affect the mean and variance of these traits, although there were significant differences between some of the populations in food neophobia and risk taking (both in means and variances). On the other hand, both urban and rural birds exhibited a behavioral syndrome including object neophobia, risk taking and activity, whereas food neophobia was part of the syndrome only in rural birds. These results indicate that there are population differences in certain aspects of personality in house sparrows, some of which may be related to habitat urbanization. Our findings suggest that urbanization and/or other population-level habitat differences may not only influence the expression of personality traits but also alter their inter-individual variability and the relationships among them, changing the structure of behavioral syndromes.     

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.     

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.     

Urbanization,nestling growth and reproductive success in a moderately declining house sparrow population

Ecological conditions are likely to change with increasing urbanization, influencing the demography and size of animal populations. Although one of the most tightly linked species to humans, the house sparrow has been suffering a significant decline worldwide, especially in European cities. Several factors have been proposed to explain this conspicuous loss of urban sparrows, but studies evaluating these factors are usually restricted to Britain where the decline was very drastic, and it is unclear whether similar or different processes are affecting urban populations of the species elsewhere. In this study we investigated the reproductive success of urban and rural sparrows in a central European country, Hungary where our census data indicate a moderate decline during the last decade. We found that rural pairs produced more and larger fledglings than suburban pairs, and the difference remained consistent in two years with very contrasting meteorological conditions during breeding. This difference is likely explained by habitat differences in nestling diet, because we found that 1) rural parents provided large prey items more often than suburban parents, 2) birds from differently urbanized habitats produced fledglings of similar number and size in captivity under identical rearing conditions with ample food for nestlings, and 3) in a cross‐fostering experiment, nestlings tended to grow larger in rural than in suburban nests irrespective of their hatching environment. These results agree with those found in a recent British study, indicating that poor nestling development and survival due to inadequate diet may be widespread phenomena in urbanized habitats.     

Migratory New World Blackbirds (Icterids) Are More Neophobic than Closely Related Resident Icterids

Environments undergo short-term and long-term changes due to natural or human-induced events. Animals differ in their ability to cope with such changes which can be related to their ecology. Changes in the environment often elicit avoidance reactions (neophobia) which protect animals from dangerous situations but can also inhibit exploration and familiarization with novel situations and thus, learning about new resources. Studies investigating the relationship between a species’ ecology and its neophobia have so far been restricted to comparing only a few species and mainly in captivity. The current study investigated neophobia reactions to experimentally-induced changes in the natural environment of six closely-related blackbird species (Icteridae), including two species represented by two distinct populations. For analyses, neophobic reactions (difference in number of birds feeding and time spent feeding with and without novel objects) were related to several measures of ecological plasticity and the migratory strategy (resident or migratory) of the population. Phylogenetic relationships were incorporated into the analysis. The degree of neophobia was related to migratory strategy with migrants expressing much higher neophobia (fewer birds feeding and for a shorter time with objects present) than residents. Furthermore, neophobia showed a relationship to diet breadth with fewer individuals of diet generalists than specialists returning when objects were present supporting the dangerous niche hypothesis. Residents may have evolved lower neophobia as costs of missing out on opportunities may be higher for residents than migrants as the former are restricted to a smaller area. Lower neophobia allows them approaching changes in the environment (e.g. novel objects) quickly, thereby securing access to resources. Additionally, residents have a greater familiarity with similar situations in the area than migrants and the latter may, therefore, initially stay behind resident species.     

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.     

Social facilitation does not reduce neophobia in Chestnut-sided Warblers (Parulinae:Dendroica pensylvanica)

Chestnut-sided Warblers (Dendroica pensylvanica) show aversion to feeding at a familiar food source if placed next to a novel object. I have suggested that neophobia is an adaptation of specialized animals to reduce wasteful exploration. In this experiment I tested whether social facilitation mitigates the fear and decreases the latency to forage at a novel foraging site. As far as I know, the effect of social factors on neophobia has not been previously investigated. Because Chestnut-sided Warblers are intraspecifically solitary during the non-breeding season, I examined their response to novel foraging sites in the presence of a Bay-breasted Warbler (D. castanea) “trainer”. Chestnut-sided Warblers commonly join flocks with this more generalized and less neophobic congener. Chestnut-sided Warblers showed no tendency to feed in the presence of a Bay-breasted Warbler that is freely feeding from the unfamiliar microhabitat. Specialized animals may be more resistant to social facilitation and observational learning than more generalized species.     

Response to Predation Risk in Urban and Rural House Sparrows

Habitat urbanization may change the density of predators, and it is often assumed that such changes lead to altered predation risk for urban populations of their prey. Although it is difficult to study predation hazard directly, behavior responses of prey species may be informative in inferring such habitat differences. In this study, we compared the risk‐taking behavior of urban and rural house sparrows (Passer domesticus) after simulated attacks by two of their important predators (sparrowhawk Accipiter nisus and domestic cat Felis catus). The birds were startled by moving dummies of these predators and respective control objects, and their risk taking was estimated as their latency to feed after the startle. We found that sparrows responded more strongly (had longer post‐startle feeding latencies) to sparrowhawk attacks than to the control object, and their responses differed between the habitats. First, risk taking of urban birds strongly decreased with age (older birds had longer latencies than young birds), while there was no such age difference in rural birds. Second, young urban birds responded less strongly, while older urban birds responded more strongly to the sparrowhawk than the same age groups of rural birds, respectively. We did not succeed in evoking antipredatory response by simulated cat attacks, because birds responded similarly to the dummy and the control object. Our results support that predation risk, posed at least by avian predators, is different in urban and rural habitats of house sparrows. The increased wariness of older, hence presumably more experienced, urban birds implies that sparrows may be more exposed to predation in cities.     

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.     

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.     

An ecological framework of neophobia: from cells to organisms to populations

Neophobia is the fear of novel stimuli or situations. This phenotype has recently received much ecological attention, primarily in the context of decision making. Here, we explore neophobia across biological levels of organisation, first describing types of neophobia among animals and the underlying causes of neophobia, highlighting high levels of risk and uncertainty as key drivers. We place neophobia in the framework of Error Management Theory and Signal Detection Theory, showing how increases in overall risk and uncertainty can lead to costly non‐responses towards novel threats unless individuals lower their response threshold and become neophobic. We then discuss how neophobic behaviour translates into population and evolutionary consequences before introducing neophobia‐like processes at the cellular level, where some phenomena such as allergy and autoimmunity can parallel neophobic behaviour. Finally, we discuss neophobia attenuation, considering how a sudden change in the environment from dangerous to safe can lead to problematic over‐responses (i.e. the ‘maladaptive defensive carry‐over’ hypothesis), and discuss treatment methods for such over‐responses. We anticipate that bridging the concept of neophobia with a process‐centered perspective can facilitate a transfer of insight across organisational levels.     

Early experience affects learning performance and neophobia in a cooperatively breeding cichlid

The ability to respond flexibly to environmental challenges, for instance by learning or by responding appropriately to novel stimuli, may be crucial for survival and reproductive success. Experiences made during early ontogeny can shape the degree of behavioural flexibility maintained by individuals during later life. In natural habitats, animals are exposed to a multitude of social and non‐social ecological factors during early ontogeny, but their relative influences on future learning ability and behavioural flexibility are only poorly understood. In the cooperatively breeding cichlid Neolamprologus pulcher, we investigated whether early social and predator experiences shape the learning performance, flexibility, and response to novelty of adults. Fish were reared either with or without parents and helpers and with or without perceived predation risk in a full‐factorial experiment. We investigated the influence of these treatments on learning performance and flexibility in a spatial acquisition and reversal learning task. To test for response to novelty, we performed a neophobia test. We found that fish reared with predator experience, but without the presence of older group members outperformed fish with other rearing backgrounds in reversal learning and that individuals, which had been reared in a socially more complex environment together with older group members responded less neophobic toward a novel object than individuals reared among siblings only. Comparative evidence from fish and rats suggests that these developmental effects may be driven by the cues of safety perceived in the presence of guarding parents.     

The Significance of Ecological Factors for Exploration and Neophobia in Parrots

Exploratory behaviour plays an important role in most animals for gathering information about their environment. If it constitutes an adaptation to different environmental conditions exploratory behaviour should differ between species. This has been tested with several hypotheses.
Sixty-one parrot species (Psittacidae) from eight tribes with different diets and habitat preferences were investigated in aviaries. Two tests were carried out. First, a novel object (wooden ring) in the familiar aviary was presented on two test days in the exploration test. Latencies until first contact with the object and the duration of exploration were recorded. Secondly, in the neophobia test, novel objects were placed beside the feeding dish and latencies until first food intake were recorded.
The exploration and neophobia data were related to 12 (13) ecological variables using multiple regression analyses. Phylogenetic relationships were considered.
Species that inhabit complex habitats, such as forest edges, or that feed on buds or species from islands showed the shortest latencies in the exploration test. In contrast, long latencies were related to a diet including a great amount of seeds and/or flowers. The longest duration of exploration occurred in species eating nuts or originating from islands, whereas short durations were related to feeding on seeds. Neophobia was positively related to a diet consisting of insects, and negatively to a diet of leaves. There was no relationship between measures of exploration and neophobia. Exploration and neophobia seem to be tightly related to the ecology of a species.     

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.     

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.     

Lean birds in the city: body size and condition of house sparrows along the urbanization gradient

1. Urbanized habitats differ from natural ones in several ecological features, including climate, food availability, strength of predation and competition. Although the effects of urbanization on avian community composition are well known, there is much less information about how individual birds are affected by these human-generated habitat differences. 2. In this study we investigated the relationships between the morphological characteristics and the degree of habitat urbanization in house sparrows, Passer domesticus (Linne 1758) . We collected data for more than 1000 non-breeding adult birds in Hungary between 1997 and 2006, from seven sites including farmlands, suburban areas and city centres. 3. We found that the body mass, tarsus length and body condition of free-living sparrows differed among the sites: birds in more urbanized habitats were consistently smaller and in worse condition than birds in more rural habitats. A composite measure of habitat urbanization (based on building density, road density and vegetation cover) explained over 75% of variance between sites in the studied traits, after we controlled for the effects of sex, year, season and time of capture. 4. The difference in body mass between rural and urban sparrows was significant when birds were kept in aviaries under identical conditions, with constant ad libitum food availability. It is therefore unlikely that the reduced body size and condition of urban sparrows are a consequence of reduced access to food for adults (e.g. due to strong competition), or their short-term responses to high food predictability (e.g. by strategic mass regulation). 5. We suggest that habitat differences in nestling development or adaptive divergence of sparrow populations due to distinct environmental conditions (such as differing predation pressure) may account for the differences along the urbanization gradient.     

A taste for novelty in invading house sparrows, Passer domesticus

One of the central questions in invasion biology involves whysome introductions succeed and others fail. Although severalcorrelates of invasion success have been identified, patternsalone cannot identify the mechanisms underlying the invasionprocess. Here, we test the hypothesis that one predictor ofinvasion success, behavioral flexibility, is different betweeninvading and established populations of the same species ofbird. We predicted that neophobia (fear of novelty), a surrogateof behavioral flexibility, would be weaker in an actively invadingpopulation (28 years resident; Colon, Republic of Panama) ofhouse sparrows (Passer domesticus) compared to a populationthat had been resident for more than 150 years (Princeton, NewJersey, USA). To test this hypothesis, we compared latency toconsume novel foods and phobia of novel objects between populationswhen both were kept under similar environmental conditions incaptivity. As predicted, birds from the 150-year-old populationtook significantly longer to approach and consume novel foodsthan birds from the 28-year-old population. Responses to novelobjects were not different between populations however; bothpopulations fed more readily near some novel objects, whichto our knowledge is the first such occurrence in a wild vertebratespecies. Overall, a predilection for trying new foods and beingattracted to novel objects may in part explain how this specieshas so successfully invaded new areas.     

Provision of supplementary food for wild birds may increase the risk of local nest predation

In countries such as the UK, USA and Australia, approximately half of all households provide supplementary food for wild birds, making this the public's most common form of active engagement with nature. Year‐round supplementary feeding is currently encouraged by major conservation charities in the UK as it is thought to be of benefit to bird conservation. However, little is understood about how the provision of supplementary food affects the behaviour and ecology of target and non‐target species. Given the scale of supplementary feeding, any negative effects may have important implications for conservation. Potential nest predators are abundant in urban areas and some species frequently visit supplementary feeding stations. We assess whether providing supplementary food affects the likelihood of nest predation in the vicinity of the feeder, by acting as a point attractant for potential nest predators. We provided feeding stations (empty, peanut feeder, peanut feeder with guard to exclude potential nest predators) in an area of suburban parkland in the UK and monitored the predation rate of eggs placed in artificial nests located at distances that replicated the size of typical suburban gardens. Nest predators (Magpies Pica pica, Grey Squirrels Sciurus carolinensis) were frequent visitors to filled feeders, and predation caused by Magpies, European Jays Garrulus glandarius and Grey Squirrels was significantly higher when nests were adjacent to filled feeders. The presence of a feeder guard did not significantly reduce nest predation. As supplementary feeding is becoming increasingly common during the breeding season in suburban habitats, we suggest that providing point attractants to nest predators at this time may have previously unconsidered consequences for the breeding success of urban birds.