Deactivation of dietary wariness through experience of novel food

When a forager encounters an unfamiliar type of food, it mustdecide whether to eat it and risk being poisoned or avoid eatingit and risk forfeiting a potentially valuable resource. Birdstypically respond to such situations with "dietary wariness";they show a transient aversion to approaching new food (neophobia),and many individuals also show a much longer lasting reluctanceto consume the new food (dietary conservatism), even once neophobiahas waned. Very little is known about how these processes, togethertermed "wariness," are controlled. We therefore present a seriesof experiments investigating how wariness of novel foods indomestic chicks, Gallus gallus domesticus, can be deactivatedand reactivated by different experiences of colored foods, varyingin their degree of novelty and palatability. We found that priorexperience of a single novel color of palatable chick crumbswas sufficient to deactivate both neophobia and dietary conservatismof any other novel color of crumbs tested. Relatively littleprior experience of a novel training food was needed to deactivateneophobia, after which the birds would peck at any other novelfood. In contrast, much more extensive experience of eatinga novel training food was needed before the birds would incorporateother novel foods into their diet. Chicks needed direct physicalcontact with the training food before they overcame their warinessto eat another novel food. However, observational learning wassufficient to encourage them to peck at the food (overcomingtheir neophobia). Reinstating wariness was much more easilyachieved than its deactivation. We discuss these surprisingresults in relation to the foraging behavior of wild and domesticbirds.     

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.     

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.     

Maternal presence and environmental enrichment affect food neophobia of piglets

Young omnivores show food neophobia in order to avoid the potential harmful effects of ingesting unfamiliar food items. We investigated whether the presence of the mother and an enriched rearing environment would reduce food neophobia in piglets. A mother may provide information on suitable food types to include in the diet, whereas an enriched environment may stimulate behavioural development and reduce reactivity towards novel stimuli (including food). Five barren-reared or enriched-reared piglets per litter were exposed to two novel food items in the presence, and the other five per litter in the absence, of the mother in a 7 min test. Maternal presence reduced food neophobia profoundly as reflected in a reduced latency to touching the food, a higher proportion of piglets sampling the two different food items and a higher intake. Latency to touch the food, however, was affected by maternal presence more strongly for barren-reared piglets than for enriched-reared piglets, and in the absence of the sow, consumption of one novel food type and time spent in the feeding area were higher for enriched-reared piglets.Environmental enrichment does have the potential to reduce food neophobia, but the presence of the mother during the encounter with novel food seems more efficient in decreasing food neophobia of piglets.     

Development of responsiveness to novel objects in the titi monkey,Callicebus moloch

Adult titi monkeys react to novelty more strongly and cautiously than other New World primates. Developmental changes in responsiveness were assessed by presenting complex novel objects to family groups consisting of 11 male-female pairs and their adult (31–33 months), subadult (20–23 months), and juvenile offspring (10–16 months). Food and a simple block were included as control conditions. Differences in attraction to novel objects were inversely related to age. Juveniles approached more objects, more quickly, and spent more time near them than older subjects. Parents, the least responsive age-group, seemed more indifferent than cautious. Age-effects were smaller with the block, and negligible with food. Even in the most responsive age-group, investigatory behavior appeared subdued as compared to other primate species. sensuHershkovitz, 1963.     

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.     

Food Neophobia and Social Learning Opportunities in Great Apes

Finding food resources and maintaining a balanced diet are major concerns for all animals. A compromise between neophobia and neophilia is hypothesised to enable animals to enlarge their diet while limiting the risk of poisoning. However, little is known about how primates respond to novel food items and whether their use is socially transmitted. By comparing how four different species of great apes respond to novel food items, we investigated how differences in physiology (digestive tract size and microbial content), habitats (predictability of food availability), and social systems (group size and composition) affect their response toward novelty. We presented two familiar foods, one novel fruit, four novel aromatic plants from herbal medicine, and kaolin to captive chimpanzees (Pan troglodytes), western gorillas (Gorilla gorilla), Bornean orangutans (Pongo pygmaeus) and Sumatran orangutans (Pongo abelii). We recorded smelling, approach-taste delays, ingestion, interindividual observations, and food transfers with continuous sampling. We found that behaviors differed between the apes: chimpanzees were the most cautious species and observed their conspecifics handling the items more frequently than the other apes. Close observations and food transfers were extremely rare in gorillas in comparison to orangutans and chimpanzees. We suggest that a low neophobia level reflects an adaptive response to digestive physiological features in gorillas and to unpredictable food availability in orangutans. Social interactions appeared to be predominant in chimpanzees and in both orangutan species to overcome food neophobia. They reflect higher social tolerance and more opportunities for social learning and cultural transmission in a feeding context.     

Response Toward Novel Foods and Novel Objects in Wild Cebus apella

Animals respond to novel stimuli via explorative or neophobic behavior or both. The coexistence of these responses toward novel foods may be a successful adaptive strategy for a generalist species such as Cebus apella, because it allows the gradual introduction of new foods into the diet and reduces the risk of poisoning by ingestion of large amounts of toxic compounds (Glander, 1982; Milton, 1993; Visalberghi, 1994). Neophobia has been studied mostly in captivity. We investigated responsiveness to novelty in a group of 25–30 wild tufted capuchins (Cebus apella) in Iguazü National Park (Argentina). They had been habituated to visiting sites where bananas were provided on three elevated platforms. We presented novel stimuli on an adjacent platform. There were 4 experimental conditions with 10 sessions each: the Novel Food condition, the Novel Object condition, the Control condition, in which the platform was empty, and the Banana condition. In the Novel Food and Novel Object conditions, a new stimulus—food or object—was on the platform during each session. The Banana condition provided information on capuchin response to a familiar preferred food. Overall, capuchins were less responsive toward novel objects than toward novel foods; however, although cautious, they ate small amounts of the novel foods. Age affected individual responsiveness toward novel foods, whereas sex affected responsiveness toward novel objects. Capuchins ignored the empty platform. Our findings are in agreement with the idea that tufted capuchins can adapt to new habitats by gradually exploiting new food sources.     

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.     

Neophobia and Dietary Conservatism:Two Distinct Processes?

Birds show distinct hesitation when approaching novel food and this has been termed ‘neophobia’. In laboratory-held birds like domestic chicks this effect lasts for a matter of a few minutes at most, but hesitant attack of novel foods can last for weeks or even months in wild birds. This effect, called ‘dietary conservatism’, seems to be a different type of learning process from neophobia as first described and has hitherto been largely overlooked. This paper presents some evidence for the view that the processes may be fundamentally different. We outline results from laboratory chicks that show neophobia to be easily deactivated by experience, which renders it unlikely to be an important force in wild birds. We also report evidence that the process of incorporation of novel food into the diet is not a simple one-stage process but includes at least four steps of assessment. The paper concludes with an outline of the importance of dietary conservatism in our understanding of the evolution of aposematism and the workings of mimicry. This revised version was published online in July 2006 with corrections to the Cover Date.     

Brood division in robins

Broods of fledgling robins Erithacus rubecula are sometimes divided between their parents so that each parent feeds only some of the chicks. These associations between a parent and certain of its young (‘family units’) are shown to be stable over periods of days. Brood division is most frequent in broods that are not followed by another nesting attempt. Experimental manipulation of the food supply suggests that brood division is relaxed when food is readily available. An analysis of the interactions between parents and chicks demonstrates that both adults and fledglings play a role in brood division. The possible functions of brood division are discussed with reference to ‘other types of care’, ‘parental efficiency’, ‘cheat countermeasure’ and ‘two types of chick’ hypotheses. Male parents feed chicks with shorter winglengths than do females: since females tend to have shorter winglengths than males, this suggests that chicks are cared for by parents of the opposite sex. Possible causes and consequences of this observation are discussed.     

Novelty effects in a multimodal warning signal

The warning signals of toxic insects are often 'multimodal', combining bright coloration with sounds or odours (or both). Pyrazine (a common insect warning odour) can elicit an intrinsic avoidance in domestic chicks Gallus gallus domesticus, both against novel coloured food, and also against food colours that are specifically associated with aposematism, namely yellow and red. In three experiments, we investigated the role of novelty in this innate bias against yellow coloured food in the presence of pyrazine. Naive chicks were familiarized either to pyrazine odour or to coloured food before being tested for a bias against yellow (warningly coloured) food as opposed to green (nonwarningly coloured) food. In experiment 1, pyrazine novelty was shown to be vital for eliciting a bias against yellow food. However, experiment 2 suggested that colour novelty was not important: chicks familiarized with coloured crumbs still avoided yellow crumbs when pyrazine was presented. In a third experiment that gave chicks an even greater degree of pre-exposure to coloured crumbs, the bias against yellow food eventually waned, although pyrazine continued to elicit an aversion to yellow even after birds had had experience of up to 24 palatable yellow crumbs. Pyrazine novelty has been an important pressure in the evolution of multimodal warning signals, and can continue to promote the avoidance of warningly coloured food, even when it is relatively familiar. The implications for warning signals are discussed. Copyright 1999 The Association for the Study of Animal Behaviour.     

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.     

Hormonal Correlates of Dominance and Starvation-induced Aggression in Chicks of the Blue-footed Booby

In the blue-footed booby (Sula nebouxii), the first-hatched chick aggressively dominates its sibling and sometimes kills it when food is in short supply. To investigate the endocrine correlates of dominance-subordinance and hunger-induced agonism, we deprived 15–20-d-old single-chick and two-chick broods of food during 48 h by taping chicks' necks to prevent ingestion of parentally provided food (a protocol used previously and known to elicit escalated sibling fighting). We monitored weight and levels of circulating testosterone, oestradiol and corticosterone in deprived and normally fed broods comprising singletons, seniors (= dominants) and juniors (= subordinates), and observed behaviour to verify that aggression increased in deprived two-chick broods. During the 2 d of fasting, experimental chicks lost on average 6% of their baseline weight. After normal feeding was reinstated, seniors and singletons recovered normal (control) weight, but juniors remained significantly lighter than controls. No testosterone was detected in any nestling, but baseline corticosterone level was 109% higher in juniors than in seniors or singletons, implying that elevated corticosterone in juniors is a consequence of social subordination and may facilitate submissive behaviour. Although there was evidence that aggression of seniors increased under food deprivation, the increase was not accompanied by the rise in levels of testosterone expected under the ‘Challenge hypothesis’ (Wingfield et al. 1990). This result implies that this hypothesis probably does not apply to booby nestlings in the context of starvation-induced aggression. During the 2 d deprivation period, corticosterone levels of experimental chicks increased significantly, then declined to baseline levels a day after tapes were removed. The increase was probably due to the combined effects of starvation and frustration. We suggest that corticosterone could alter responsiveness of nestling blue-footed boobies to external stimuli, resulting in more aggression by dominants and greater readiness of subordinates to submit.     

Food-neophobia in semi-free ranging rhesus macaques: effects of food limitation and food source

This study characterizes food neophobia in semi-free ranging rhesus macaques. In experiment one, monkeys received novel and familiar foods during periods of normal provisioning and when provisioning was suspended. The monkeys did discriminate between novel and familiar foods and continued to exhibit neophobia when provisioning was suspended. In experiment two, food was either tossed to subjects or placed in the habitat so that monkeys discovered food without the observer in close proximity. Rhesus macaques were more likely to eat a novel food that was hand-tossed to them compared to food they discovered in their habitat. This study suggests that food neophobia is a robust trait in rhesus macaques and that a history of provisioning may affect the expression of the trait.     

Field but not lab paradigms support generalisation by predators of aposematic polymorphic prey: the Oophaga histrionica complex

The persistence of novel aposematic forms, and thereby the evolution of aposematic polymorphism, remain intriguing. Novel and rare forms could be disproportionally attacked by predators that already learned to avoid a pre-existing and more common aposematic form. Alternatively, novel forms could be less frequently attacked if predators are reluctant to attack unknown potential prey (neophobia) or if previous learning allows them to generalise and recognise the novel form as toxic. We used colour variation in polymorphic poison frogs (Oophaga histrionica complex) to test whether predators familiar with one aposematic form do generalise their avoidance behaviour to other aposematic forms. To strengthen our inference, we combined a field test of attack rates to local and non-local models with a lab experiment of generalisation capabilities by newly born chicks. Field predators attacked a significantly lower proportion of 529 aposematic compared to 150 cryptic models. Predators co-occurring with the local aposematic form of O. histrionica equally avoided non-local forms, especially in areas where the species was abundant. Forty-two lab chicks learned to discriminate between an aposematic and a cryptic image, but failed to generalise to other aposematic images, even though we tried with six combinations of aposematic forms. To better mimic the situation in the field, we further tested whether chicks trained with a set of four simultaneous aposematic images would generalise better. They failed to learn the discrimination task. Our data contrast with previous field studies on other poison frogs, and support a role for generalisation, and arguably not neophobia, in predator avoidance of novel aposematic forms.     

Response toward novel stimuli in a group of tufted capuchins (Cebus libidinosus) in Brasília National Park, Brazil

We investigated responses toward novel foods and novel objects by wild capuchins that routinely exploit visitors' foods in Brasília National Park. Given the capuchins' daily exposure to human foods and objects, we expected them to be more explorative toward novel foods and objects compared to capuchins that are not habituated to visitors. However, since the safety and palatability of potential foods have to be learned, we also expected the capuchins to be cautious about eating novel foods, as has been reported for wild and captive capuchins. Stimuli were presented on a platform in four experimental conditions: familiar food (FF), novel food (NF), familiar food plus novel object (FF+O), and novel food plus novel object (NF+O). Latencies to approach and contact the platform, and to approach and to ingest food did not differ across conditions. Nevertheless, the capuchins were significantly more responsive (measured in terms of interest, manipulation, etc.) toward familiar foods than novel foods, and ate significantly more of the former. In other words, their explorative response toward novel foods led to little consumption. Our results do not support the "readiness to eat" hypothesis, according to which a lower readiness to eat and food neophobia are the consequences of the presence of a distracting novel object. The finding that capuchins explore novel stimuli but remain cautious about eating novel foods supports the view that neophilia and neophobia are motivationally independent responses.     

Spatial Neophilia and Spatial Neophobia in Resident and Migratory Warblers (Sylvia)

Residents and migrants use their environment very differently – the former remain in a given habitat throughout the year, whereas the latter are repeatedly confronted with unfamiliar environments. The difference in ecology may influence decision-making processes whether, when and to which extent to explore an unfamiliar environment. We have investigated spatial neophobia and spatial neophilia – two important novelty reactions that may underlie decision-making – in two closely related warbler species, the resident Sardinian warbler and the migratory garden warbler. Individuals of both species could access an unfamiliar room from a familiar cage. We assessed the conflict between the motivation to enter the novel room (spatial neophilia) and the motivation to avoid it (spatial neophobia) as the frequency and duration of perching on the dowel in the cage, which led to the unfamiliar room before entering it. Furthermore, we measured the latency to enter the novel room and compared the number of individuals of each species entering the room. The combination of the parameters measured allowed assessing the degree of both neophobia and neophilia. Finally, the time spent on each branch in the novel room was taken as a measure for spatial exploration. The migrants perched less often and spent less time on the dowel leading to the room, and entered the novel room quicker than the residents. Additionally, more migrants than residents entered the room. The migrants' decision to enter the novel room can best be explained with a combination of low spatial neophobia coupled with high spatial neophilia, whereas the residents' decision-making is best explained with high spatial neophobia coupled with high spatial neophilia. The differences in neophobia support the migrant-neophobia hypothesis. When in the room, the migrants spent less time on each branch than the residents, possibly indicating that the former collect less spatial information than the latter.     

Does the environmental background (intensive v. outdoor systems) influence the behaviour of piglets at weaning?

Under intensive pig husbandry, outdoor systems offer a more complex physical and social environment compared with indoor systems (farrowing sheds). As the rearing environment affects behavioural development, it can, therefore, influence behavioural responses of pigs to stressful environments in later stages of production. We tested how the rearing environment influenced behavioural responses to a novel arena test in piglets on the day that they were weaned and mixed into large groups. We recorded video footage and compared the behavioural responses of 30 outdoor-raised and 30 farrowing shed-raised piglets tested in an experimental arena and sequentially exposed to four challenges (each for 5 min) on the day of weaning. Quantitative and qualitative behavioural measures were recorded using time budgets and scoring demeanour or ‘qualitative behavioural expression’ (using Qualitative Behavioural Assessment (QBA)). When held in isolation (challenge 1), both groups were scored as more ‘scared/worried’, while outdoor-raised piglets spent more time eating and jumping against the arena walls. Both groups interacted with a plastic ball (challenge 2: exposure to a novel object) during which they were scored as more ‘playful/curious’ than other challenges. When a food bowl was introduced (challenge 3), farrowing shed-raised piglets were more interested in playing with the food bowl itself, whereas outdoor-raised piglets spent more time eating the feed. Finally, there were no significant differences in social behaviour (challenge 4: introduction of another piglet) between the two groups in terms of the latency to contact each other, amount of time recorded engaged in aggressive/non-aggressive social interactions or QBA scores. Although piglets spent 30% of their time interacting with the other piglet, and half of this time (47%) was engaged in negative interactions (pushing, biting), the levels of aggression were not different between the two groups. Overall, outdoor-raised piglets ate more and were scored as more ‘calm/passive’, whereas farrowing shed-raised piglets spent more time investigating their environment and were scored as more ‘playful/inquisitive’. In conclusion, we did not find differences in behaviour between outdoor-raised and farrowing shed-raised piglets that would highlight welfare issues. The differences found in this study may reflect conflicting affective states, with responses to confinement, neophobia and motivation for exploration evident.