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.     

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.     

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.     

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.     

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.     

Responses of domestic chicks to novel food as a function of sex,strain and previous experience

Food neophobia or a hesitancy to feed on unfamiliar food was examined in domestic chicks as a function of genetic and experiential factors associated with differential responsiveness to novelty. Chicks were presented with novel blue mash following a regime of food withdrawal and return. ‘S’ line chicks (light hybrid) fed significantly sooner, longer and more than did medium-hybrid ‘T’ line birds and females accepted novel food more readily than males. Food neophobia was significantly reduced by previous exposure to a variety of coloured foods and by enrichment of the home environment with assorted novel objects. The results are discussed in terms of the relationship between food neophobia, general responsiveness to novelty and underlying levels of fearfulness.     

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.     

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.     

Reduced dietary conservatism in a wild bird in the presence of intraspecific competition

The presence of intraspecific competitors can increase foraging costs through exploitation of resources. Optimal foraging theory suggests that when the cost of pursuing one food type increases, alternative resources should be accepted. Accepting novel foods readily might put a competitor at an advantage over its more conservative rivals in the race for sufficient sustenance, but also opens it to the danger of poisoning by chemically protected food. Dietary conservatism is a foraging behaviour characterised by a prolonged avoidance of novel foods, long after neophobia (initial fear of novel objects) has been overcome, and so might be seen as a disadvantage to foragers in a competitive situation. There are two stable foraging strategies found within forager populations: 1) adventurous consumers (AC) which rapidly accept novel foods and 2) foragers showing dietary conservatism (DC). The expression of these two strategies may also vary with environmental conditions. The aim of this study was to investigate the effect of intraspecific competition on the levels of dietary conservatism displayed among wild caught blue tits Cyanistes caeruleus. Blue tits were offered items of both novel and familiar foods under two conditions: with a competitor and without. Our results showed that individuals who experienced competition incorporated the novel items into their diet faster than those who did not experience competition. This study demonstrates, for the first time, the degree of plasticity in the expression of the DC trait using wild birds in laboratory conditions. This plasticity represents a significant adaptation to reduce the costs of foraging conservatively when novel alternative resources should be accepted.     

Learning Differences between Feral Pigeons and Zenaida Doves: The Role of Neophobia and Human Proximity

Learning differences predicted from ecological variables can be confounded with differences in wariness of novel stimuli (neophobia). Previous work on feral pigeons ( Columba livia ), as well as on group-feeding and territorial zenaida doves ( Zenaida aurita ), reported individual and social learning differences predicted from social foraging mode. In the present study, we show that speed of learning a foraging task covaries with neophobia and latency to feed from a familiar dish in the three types of columbids. Pigeons were much faster than either territorial or group-feeding zenaida doves on all tests conducted in captivity, but showed unexpectedly strong neophobia in some urban flocks during field tests. Human proximity strongly affected performance in group-feeding doves both in the field and in captivity. They were slightly faster at learning than their territorial conspecifics in cage tests. In multiple regressions, species identity, but not social foraging mode, significantly predicted individual variation in learning, as did individual variation in neophobia. Wariness of novel stimuli and species differences associated with artificial selection appear to be more important than foraging mode and wariness of humans in accounting for learning differences between these columbids.     

Experimental analysis of diet specialization in the snail kite: the role of behavioral conservatism

We examined factors maintaining extreme diet specialization in the snail kite (Rostrhamus sociabilis), a medium-sized hawk which feed almost exclusively on Pomacea snails, by determining why during some months kites eat crabs (Dilocarcinus dentatus) in the Ilanos of Venezuela. We offered snails and crabs of different sizes to wild free-flying birds to develop estimates for a prey choice model. Handling times of Pomacea doliodes snails averaged 90±39 s and were positively correlated with snail size. Handling times for crabs (x=353±130 s) were significantly longer and exhibited greater variation than for snails, and were not correlated with crab size. Edible crab tissues had greater dry weights and contained more energy (25.37 kJ/g) than tissues of snails (16.91 kJ/g). Total energy of crabs was much greater than that of snails, and total energy of both foods was highly related to body length. We constructed an allometric equation for profitability of snails and crabs. Snails were more profitable than all but the largest crabs, but estimates of variance in profitability were greater for crabs. Predictions from the model were tested by offering crabs that represented equal, greater and much greater profitability than snails, to determine whether kites chose prey according to profitability. Only 15.6% of 289 food items chosen were crabs. Half of the 18 kites tested did not eat crabs and only 3 birds switched from snails to more profitable crabs. Four fledglings showed no preference for snails. The role of neophobia in food choice was investigated by offering unfamiliar snails (Pomacea urceus) to kites. Kites exhibited neophobic behaviors, and 5 of 12 birds chose not to capture P. urceus. Two-thirds of the 12 snails chosen were rejected immediately, but the others were handled efficiently (x=133±89 s). Although morphological adaptations allow kites to specialize on snails, the costs of specialization were overcome for kites when the profitability of alternative food increased sufficiently. Our results suggest a role for behavioral conservatism, in the form of risk-averse foraging and neophobia, in maintaining severe diet specialization in the snail kite.     

Seeing group members eating a familiar food enhances the acceptance of novel foods in capuchin monkeys

In primates, social context is one of the factors that increases the acceptance of novel foods. Previous experiments showed that tufted capuchins, Cebus apella, eat significantly more of novel foods when in the presence of group members eating the same novel foods. Several processes may have led to these results. The mere presence of group members may reduce the individual's stress of being alone, or its neophobic response and, consequently, may increase its food consumption. The individual may be influenced by what group members do, and local/stimulus enhancement and/or social facilitation may occur. To investigate the above processes, we assessed whether an individual capuchin monkey's consumption of novel foods is lower when (1) the individual is alone with nobody in the nearby cage than when (2) group members are present in the nearby cage with no food or when (3) they are present and eating a familiar food. We tested 15 subjects with three novel foods, each presented in one condition. In both social conditions, the more group members there were by the food box the more the experimental subject ate. In addition, when group members were present and eating food, there was a significant increase in the acceptance of the three foods, regardless of what group members were eating. We argue that social facilitation of eating is a quicker way to overcome neophobia and only social facilitation of eating what the others are eating can be considered a safe way to learn about a safe diet. Copyright 2000 The Association for the Study of Animal Behaviour.     

Non-warning odors trigger innate color aversions--as long as they are novel

Warning signals made by unpalatable insects to potential predatorscommonly target more than one sense: such signals are "multimodal." Pyrazines are odors produced by warningly colored insects whenattacked, and have been shown to interact with food coloration,biasing avian predators against novel and typically aposematicfood. However, at present it is not known whether this is anadaptation by prey to exploit a general feature of avian psychology,or an evolutionary response by birds to enhance their avoidanceof unpalatable prey. Here we investigate the effect of otherodors on the innate responses of naive domestic chicks (Gallusgallus domesticus) to food that is of novel color, or of acolor that is associated with warning coloration, yellow. Inthe first experiment, we demonstrate that natural and artificialodors that have no association with aposematism in the wildcan produce biases against both novel colored foods and yellowcolored foods. In a second experiment, we also show that odor novelty is vital for eliciting such effects. These results supportthe idea that warning odors have evolved in response to preexistingpsychological biases against novel odors in predators, ratherthan predators evolving specific responses against odors associatedwith unpalatable prey.     

Responses to novel foods in captive chimpanzees

Hesitancy to eat novel foods hampers the immediate enlargement of the diet but serves to limit the risk of ingesting toxic foods. Neophobia has been systematically investigated in only a few primate species, in which it appears to be affected by social influences. Surprisingly, little is known about neophobia in chimpanzees. We studied the response of eight adult captive chimpanzees to 16 foods (foods commonly eaten by humans and never tasted before by chimpanzees). Each novel food was presented twice to the chimpanzee by a familiar or an unfamiliar human. Between the two trials the human ate the food face to face with the chimpanzee (demonstration). Results showed that some foods were almost unanimously accepted, whereas others were not. Moreover, there were marked interindividual differences in food acceptance and consumption; chimpanzees ranged from being almost completely neophobic to accepting almost all foods. Familiarity with the human and the human's demonstration did not affect responses to the foods. The humans' predictions concerning the chimpanzees' acceptance of the different foods were rather good; furthermore, in seven cases out of eight the humans' preferences did not correlate with their predictions on the chimpanzees' preferences. The finding that most captive chimpanzees are initially cautious toward novel foods supports the little information there is regarding this subject in wild chimpanzees. However, the lack of influence of the humans' familiarity and demonstration on the response to food by the chimpanzees calls for more naturalistic studies, in which social influences are provided by group members. Since novel stimuli provide sensory stimulation and elicit exploration and social interest, occasional presentation of novel foods could be a promising and cheap device for feeding enrichment. Zoo Biol 21:539–548, 2002. © 2002 Wiley‐Liss, Inc.     

Can the dietary conservatism of predators compensate for positive frequency dependent selection against rare,conspicuous prey?

The evolution of conspicuous colouration in prey is puzzling because such coloration attracts the attention of predators. Anti-apostatic selection, in which rare prey forms are predated disproportionately often, is a second potential obstacle to the evolution of conspicuous colouration in prey, as bright novel prey forms are likely to be very rare when they first appear in populations. It has recently been postulated that dietary conservatism in predators, an extended feeding avoidance of novel prey, would allow novel conspicuous prey to survive and multiply despite anti-apostatic and conspicuousness effects. We tested this hypothesis for a novel prey type arising in an otherwise cryptic population, providing a direct test of whether anti-apostatic selection or the predators’ wariness to attack the novel prey type is the more important force acting on the novel conspicuous prey. We conducted our experiment in the “Novel World”; an experimental system designed to test predators’ foraging decisions in a large landscape. We found that the conspicuous, novel prey suffered high initial costs of conspicuousness compared with cryptic prey, since most of these prey were attacked during the first “generation”, with no opportunity to “reproduce”. However, a subset of the 17 birds (24%) were following a dietary conservative foraging strategy and they were reluctant to eat the novel prey. Interestingly these birds were not more neophobic or less explorative. Our data demonstrate how difficult it is for the novel conspicuous prey to survive in cryptic populations, but they also highlight the importance of the predator’s foraging strategies in helping to promote the evolution and maintenance of aposematism.     

Mice lacking the cell adhesion molecule Thy-1 fail to use socially transmitted cues to direct their choice of food

BACKGROUND: Thy-1 is a major cell-surface glycoprotein of mature neurons and certain other cells, including those of the lymphoreticular system. Despite being the simplest member of the immunoglobulin superfamily, the biological role of Thy-1 has proved elusive. Analysis of Thy-1 null mice has shown the presence of excessive GABAergic inhibition of neurotransmission in the dentate gyrus of the hippocampal formation selectively, without any neurological or behavioural effects being apparent. RESULTS: We show here that Thy-1 null mice are unable to make the appropriate dietary choice in the test for social transmission of food preference, despite showing a normal level of social interaction with the demonstrator mouse, normal neophobia, and normal learning in a T-maze using scented food as cues. The mice also performed normally in tests of anxiety, locomotor activity, exploration of a novel environment, habituation to novelty and spatial learning. This phenotype is maintained on two different strain backgrounds, is rescued by transgenic expression of Thy-1 and by administration of the GABA(A) receptor antagonist pentylenetetrazole. CONCLUSIONS: The test for social transmission of food preference is based on the normal ability of mice in a colony to learn from each other which foods are safe to eat. The lack of this key survival behaviour in Thy-1 null mice could act as an evolutionary pressure point to conserve expression of Thy-1. Furthermore, the specific cognitive defect caused by inactivation of the Thy-1 gene suggests that it would be worthwhile to determine the role of Thy-1 in certain human familial forms of mental retardation that map to chromosome 11q22-23 in the region of the Thy-1 locus rather than the nearby ataxia telangiectasia locus.     

The effects of cache loss on choice of cache sites in black-capped chickadees

Food-storing birds lose a great deal of their stored food toother animals. We examined whether blackcapped chickadees (Parusairicapillus) modify their choice of cache sites using informationthat predicts cache loss. In experiment 1, birds learned toavoid caching at spatial locations where cache loss had previouslyoccurred, but they did not avoid caching near local color cuesthat predicted cache loss. Birds did not modify their generaluse of space in the aviary. Birds also learned to reduce searchingfor caches where spatial location predicted cache loss. Experiment2 confirmed the birds’ ability to discriminate among thespatial locations and the local color cues used in experiment1. In experiment 3, learning a food-rewarded approach to potentialcache sites occurred without any change in the choice of sitesfor caching. We discuss how chickadees selectively associatethe choice of cache site with its consequences, even over delaysof several hours between caching and cache recovery.     

Ontogenetic development of conditioned food aversion in chickens

Development of conditioned food aversion (CFA) was studied in 25-, 35-, and 45-day Leghorn chicks. Food-deprived birds had 10-min access to normal food on days 1 and 2, and to green coloured food CS on day 3. Injection of LiCl (0.15 M, 3–4% body weight) administered 10 min after CS on day 3 served as the US. Control groups were injected with the same volume of saline. Retention was tested on day 4 in three 3-min presentations of normal food alternating with two presentations of green food. Number of pecks and amount of food consumed were measured. Significant neophobic rejection of green food was observed in 25- but not in 35- and 45-day-old control birds. Neophobia in the youngest chicks was further accentuated by CFA which could be observed in pure form in the 45-day-old experimental group. Comparison of pecking rate and food intake showed that CFA in younger birds was accomplished predominantly by inhibition of pecking, and in older birds also by reduction of peck volume. It is concluded that protection against poisoning in chickens shifts between 25 and 45 days of posthatching age from neophobia to CFA.     

Pregnancy in goats does not influence intake of novel or familiar foods with or without toxins

Some hypothesize that mammals decrease intake of foods that contain toxins during pregnancy to protect the fetus. We conducted a longitudinal study of feeding behavior to determine if pregnancy-related changes in food selection and intake occurred in goats. Goats eat modest amounts of toxic plants, some of which contain teratogenic or abortifacient compounds, but it is not known if pregnant and non-pregnant goats differ in food selection. The embryo is susceptible to toxins during all stages of pregnancy, but especially so during organogenesis early in pregnancy. Thus, we hypothesized that food selection and intake by pregnant versus non-pregnant goats may differ during various stages of pregnancy. We examined the following predictions that stem from this hypothesis: relative to non-pregnant goats, pregnant goats may alter selection of familiar foods that contain toxins, and of familiar and unfamiliar foods that do not contain toxins. We fed 14 plants with known or probable teratogenic properties during two pregnancies. We also offered beet pulp containing 0.5% LiCl during one pregnancy to test for increased sensitivity to toxins. In addition, we offered novel foods several times during one pregnancy to test for increased food neophobia or neophyllia. Finally, we measured intake of the basal ration by pregnant and non-pregnant goats daily throughout both pregnancies. Both pregnant and non-pregnant goats ate modest amounts of the plants with toxins and of beet pulp with LiCl. Both groups limited intake of novel foods and beet pulp with LiCl to the same degree. Finally, pregnant and non-pregnant goats did not differ in intake (per kg MBW) of the basal ration—dry matter, energy, or protein—in either pregnancy. Thus, the data do not support the notion that goats experienced pregnancy-related changes in food selection or intake.     

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.