Food Aversion Plus Odor Cue Protects Crop From Wild Mammals

Abstract: Wild mammals cause foraging damage to crops worldwide and nonlethal methods are required for controlling such damage. Many wildlife management situations demand protection of untreated foods. We tested learned food aversion plus an odor cue as a paradigm for protecting untreated model crop items from European badgers (Meles meles). Following conditioning with a combination of ziram and clove oil, badgers avoided untreated maize cobs in presence of a clove odor cue. A clove oil control did not condition badgers. This work has been an important step before proceeding to full-scale field trials for protecting growing crops on a wider scale. (JOURNAL OF WILDLIFE MANAGEMENT 72(3):785–791; 2008)     

Levamisole can reduce bait monopolization in wild red foxes Vulpes vulpes

1. Baits are used worldwide to deliver vaccines, contraceptives and poison to wild animal species. In carnivores, multiple bait uptake and bait monopolization by dominant individuals may reduce baiting effectiveness. This study investigated whether a conditioned‐taste‐aversion agent, levamisole, can be used to decrease bait consumption by individual wild foxes Vulpes vulpes. 2. The results indicated that after consuming levamisole‐treated baits, foxes avoided eating treated baits but consumed untreated baits. We concluded that the reduction in bait consumption was achieved through learned aversion to levamisole rather than via conditioned‐taste‐aversion to baits. Adding levamisole to baits could potentially be used to reduce bait monopolization by individual wild foxes.     

Innate food aversions and culturally transmitted food taboos in pregnant women in rural southwest India: Separate systems to protect the fetus?

Pregnancy increases women's nutritional requirements, yet causes aversions to nutritious foods. Most societies further restrict pregnant women's diet with food taboos. Pregnancy food aversions are theorized to protect mothers and fetuses from teratogens and pathogens or increase dietary diversity in response to resource scarcity. Tests of these hypotheses have had mixed results, perhaps because many studies are in Westernized populations with reliable access to food and low exposure to pathogens. If pregnancy food aversions are adaptations, however, then they likely evolved in environments with uncertain access to food and high exposure to pathogens. Pregnancy food taboos, on the other hand, have been theorized to limit resource consumption, mark social identity, or also protect mothers and fetuses from dangerous foods. There have been few tests of evolutionary theories of culturally transmitted food taboos.We investigated these and other theories of psychophysiological food aversions and culturally transmitted food taboos among two non-Western populations of pregnant women in Mysore, India, that vary in food insecurity and exposure to infectious disease. The first was a mixed caste rural farming population (N = 72), and the second was the Jenu Kurubas, a resettled population of former hunter-gatherers (N = 30). Women rated their aversions to photos of 31 foods and completed structured interviews that assessed aversions and socially learned avoidances of foods, pathogen exposure, food insecurity, sources of culturally acquired dietary advice, and basic sociodemographic information. Aversions to spicy foods were associated with early trimester and nausea and vomiting, supporting a protective role against plant teratogens. Variation in exposure to pathogens did not explain variation in meat aversions or avoidances, however, raising some doubts about the importance of pathogen avoidance. Aversions to staple foods were common, but were not associated with resource stress, providing mixed support for the role of dietary diversification. Avoided foods outnumbered aversive foods, were believed to be abortifacients or otherwise harmful to the fetus, influenced diet throughout pregnancy, and were largely distinct from aversive foods. These results suggest that aversions target foods with cues of toxicity early in pregnancy, and taboos target suspected abortifacients throughout pregnancy.     

Social learning influences the preferences of domestic hens for novel food

It has been argued that social learning helps animals either avoid noxious substances or identify food items, but evidence suggests that avian social learning is fundamentally different from that of mammals. In two experiments, we investigated whether the preferences of domestic hens, Gallus g. domesticus, for novel food were influenced by observing the feeding behaviour of conspecifics. In experiment 1, we attempted to confirm that birds can develop socially learnt aversions to unpalatable foods. Despite demonstrators showing a highly visible ‘disgust reaction’ after eating unpalatable coloured food, observers did not develop aversions to similarly coloured food. In experiment 2, we aimed to determine whether preferences for palatable food were socially learnt, and whether the extent of a demonstrator's preference for novel food affected the magnitude of the observer's socially learned preference. Demonstrators ate coloured food of standard or high palatability, or did not peck food at all. When the demonstrators pecked more frequently or fed more quickly from the food, the observers consumed a greater proportion of food of the same colour; however, this was only when the food was red, not green. We argue this indicates an unlearned aversion to red food, overcome by social learning of the food being highly palatable. The results provide no evidence that adult hens learn aversions through observing disgust reactions, but show that hens are sensitive to the extent of demonstrator preferences for palatable food. The data do not support the hypothesis that avian social learning is fundamentally different from that of mammals. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Learned Recognition of Novel Predator Odour by Zebra Danios, Danio Rerio, Following Time-shifted Presentation of Alarm Cue And Predator Odour

Fishes in the superorder ostariophysi possess specialized epidermal cells that contain an alarm cue. Fish associate novel odours, such as the odour of a predator, with predation risk after a single, simultaneous exposure to the novel odour and alarm cue. Thereafter, the novel cue is recognized as an indicator of risk and its presence induces antipredator behaviour. Two common antipredator behaviours are reduction in activity and movement to the bottom. This phenomenon has been demonstrated many times in the laboratory setting for a variety of aquatic taxa. In nature however, the detection of novel predator odour may be time-shifted with respect to the detection of alarm cues. Is there a critical period immediately upon the detection of alarm cue in which associative learning can occur? We presented zebra danios, Danio rerio, with the odour of northern pike, Esox lucius, 5?min after presenting them with either alarm cue or water (control). During a predation event, 5?min is a long time. When later retested with pike odour alone, zebra fish conditioned with alarm cue significantly increased antipredator behaviour in terms of decreased activity and movement towards the bottom. Control fish did not recognize pike odour as dangerous when retested. These data show that learned recognition of predation risk is sufficiently robust to accommodate ecologically realistic temporal shifts in stimulus presentation.     

An Epidemic of Sylvatic Rabies in Finland

When rabies reappeared in Finland in April 1988, the country had been rabies free since 1959. Soon a picture of sylvatic rabies become evident, its main vector and victim being the raccoon dog (Nyctereutes procyonoides). Between 8 April 1988 and 16 February 1989, 66 virologically verified cases were recorded (48 raccoon dogs, 12 red foxes, 2 badgers, 2 cats, l dog and 1 dairy bull) in an area estimated at 1700 km2 in south-eastern Finland. The greatest distance between recorded cases was 67 km. A positive reaction with monoclonal antibody p-41 indicated that the virus was an arctic-type strain. A field trial on oral immunization of small predators was initiated in September 1988 using Tübingen fox baits according to the Bavarian model of bait distribution. Each bait contained 5*107 TCID50/ml modified live rabies virus (SAD-B19). The 6 months’ surveillance indicate a seroconversion rate of 72% (N=126) in the raccoon dog population, 67% (N=56) in the red foxes and 13% (N=16) in the badgers, when titers ≥1.0 IU/ml are considered seropositive. In the whole follow-up period, no statistically significant difference could be detected between the raccoon dogs and red foxes in the rate of seroconversion or in the uptake of tetracycline from the baits. Notably high antibody levels were recorded in both raccoon dogs and red foxes within 4–5 months after vaccination. Of the seropositive animals, the proportion of animals with titers 3.0 IU/ml or greater was higher in raccoon dogs (73%) than in red foxes (51%) (x2= 5.29, p< 0.05). The trial shows that raccoon dogs can be immunized against rabies in the field with vaccine baits originally developed for controlling sylvatic rabies in foxes.     

Parallel reinforcement pathways for conditioned food aversions in the honeybee

Avoiding toxins in food is as important as obtaining nutrition. Conditioned food aversions have been studied in animals as diverse as nematodes and humans [1, 2], but the neural signaling mechanisms underlying this form of learning have been difficult to pinpoint. Honeybees quickly learn to associate floral cues with food [3], a trait that makes them an excellent model organism for studying the neural mechanisms of learning and memory. Here we show that honeybees not only detect toxins but can also learn to associate odors with both the taste of toxins and the postingestive consequences of consuming them. We found that two distinct monoaminergic pathways mediate learned food aversions in the honeybee. As for other insect species conditioned with salt or electric shock reinforcers [4-7], learned avoidances of odors paired with bad-tasting toxins are mediated by dopamine. Our experiments are the first to identify a second, postingestive pathway for learned olfactory aversions that involves serotonin. This second pathway may represent an ancient mechanism for food aversion learning conserved across animal lineages.     

The effects of red fox Vulpes vulpes faecal odours on the feeding behaviour of Orkney voles Microtus arvalis

Orkney voles Microtus arvalis show avoidance of red fox Vulpes vulpes faecal odours, both in the laboratory and in the wild. Since these voles have been isolated from foxes since Neolithic times it is likely that these responses are innate rather than learned.
When applied to young Scots pine saplings, the fox odour inhibited feeding by voles when alternative foods were available.     

Avoidance of potentially harmful food cannot be socially transmitted between rats

The social transmission of food preferences(STFP) is a behavioural task of olfactory memory, in which an observer rat learns safe food odours from a demonstrator rat, and shows preference for this odour in a subsequent choice test. However, previous studies have failed to detect the transmission of information about food of potential danger and food aversion using STFP test. In this study, we tested how demonstrators' health affects the exchange of odour information and whether observers can learn danger information from an unhealthy demonstrator. As expected, the observer rat formed an odour preference after interacting with a demonstrator rat that had just eaten food containing a new odour, however, odour preference rather than aversion was also formed after interacting with a demonstrator rat injected with LiCl(used to induce gastric malaise). Furthermore, anaesthetized demonstrator rats and half-anaesthetized demonstrator rats, which showed obvious motor deficits suggesting an unhealthy state, also socially transmitted food preferences to observers. These results suggest that the social transmission of food preferences task is independent of a demonstrators' health, and that information about dangerous foods cannot be transmitted using this behavioural task.     

Bait delivery for oral rabies vaccine to gray foxes

Rabies is a widespread zoonotic disease that has reached epizootic proportions in gray foxes (Urocyon cinereoargenteus) in central Texas. Because each species of carnivore has different food preferences and foraging strategies, it is essential that the efficacy of a bait delivery program be examined for gray foxes prior to an oral vaccination program being attempted. Field trials were conducted to determine bait preferences of free-ranging gray foxes to selected baits and odor attractants. Baits consisted of polymer cubes made of either dog food meal or fish meal, and a wax-lard cake that was enhanced with marshmallow flavoring. Attractants added to baits exuded sulfurous, fatty, cheesy, or sweet odors and flavors. During 3,589 operable bait station nights, gray fox visitation and bait uptake rates were 9.2% and 8.3%, respectively. Gray foxes exhibited no preference in bait uptake rates between bait and odor attractant combinations. Gray foxes exhibited no difference in cumulative bait uptake rates between onroad and offroad sites; however, the uptake rate by raccoons was significantly greater for baits placed on roads than for baits randomly placed. Raccoons were the major non-target species competing for baits, being attributed with 73% of the total uptake. Visitation and bait uptake rates by raccoons significantly increased after a 7-day lethal removal of raccoons (n = 37) from the study area. Random distribution of baits is recommended; it reduced bait uptake by non-target species without adversely affecting uptake by gray foxes.     

Bait Uptake and Caching by Red Foxes and Nontarget Species in Urban Reserves

Abstract: The management of biodiversity in urban areas provides a challenge for conservation managers who are interested in the recovery of native species by controlling exotic species. Exotic-animal control programs using poisons can be contentious in terms of the health and safety of nontarget species, including people. Managing exotic predators in urban areas must be effective at 2 levels: controlling the target species and minimizing impacts to nontarget species. We investigated the feasibility of instigating a poison-baiting program to control nonindigenous European red foxes (Vulpes vulpes) in city conservation reserves (Perth, Australia). We selected 3 reserves to assess the safety and efficacy of baiting for foxes by maximizing bait uptake by the target species, and minimizing uptake by nontarget species. We tested 2 types of meat bait using 4 bait presentation methods (untethered, uncovered; untethered, covered; tethered, uncovered; tethered, covered). Bait uptake by foxes was highest in urban reserves compared to that in a peri-urban reserve. Bait type and presentation method equally explained bait uptake by foxes. Untethered and uncovered baits were removed 10% more often by foxes, and untethered baits had been cached more often than tethered baits. Baits cached by foxes for up to 1 week were not removed by species other than foxes. Domestic dogs and native birds were common nontarget species to remove baits. Dogs showed no aversion to removing any bait type, nor did bait presentation method influence bait removal. Birds removed fewer baits that had been tethered and covered. We provide an evidence base to demonstrate that bait uptake by nontarget species can be minimized, although we suggest that a fox control program is likely to be more of an organizational challenge to change public attitudes toward responsible dog ownership rather than a technical challenge to poison foxes.     

Memory retention of conditioned aversion training in New Zealand's alpine parrot,the kea

New Zealand pest control operations commonly deploy toxic sodium fluoroacetate (1080) baits to control introduced mammalian predators and protect vulnerable native fauna, yet the highly intelligent kea (Nestor notabilis) is at risk of mortality following ingestion of toxic baits intended for their protection. We tested the retention of conditioned aversion in 11 captive kea that had learned to avoid baits containing the bird repellent anthraquinone alongside color, olfactory, and taste cues. We revisited kea over increasing time intervals (3 days, 5 weeks, 3 months, 6 months, and 1 yr) offering them otherwise identical non-repellent baits. Kea retained their aversion until the final session, 1 year after previous exposure to reinforcement, and almost 2 years since previous exposure to repellent. Whether the kea forgot their aversion or the repeated exposures to non-repellent baits resulted in extinction of the aversion, our results indicate that kea are capable of remembering an aversion for long enough to be of practical use to conservation managers in reducing kea mortality through 1080 operations.     

A parametric study of flavoured food avoidance in chicks

It has previously been shown that the ability of the chick toassociate the consumption of novel flavoured substances withsubsequent malaise is specific to the mode of ingestion (Gilletteet al., 1980), i.e., chicks will readily form conditioned aversionsto weakly flavoured solutions but not to relatively stronglyflavoured foods. The present series of four experiments indicatedthat the failure of chicks to develop conditioned aversionsto flavoured food is not due to the parameters of flavour intensity (salience), conditioned stimulus duration, or tastequality. Altering the validity of visual cues did not facilitateflavour avoidance nor did compounding the flavour cue with avisual cue. Although chicks showed increasing neophobia forincreasing concentrations of NaCl flavoured food, they did notlearn to avoid the food relative to controls (Experiment 1).Similarly, varying the amount of time allowed for ingestingthe NaCl flavoured food produced no differences between groups(Experiment 2). Since it was possible that NaCl might produceconsiderable malaise in its own right, the third experimentwas a partial replication of Experiment 2 using sucrose flavouredfood. Again, there was no effect due to conditioned stimulusduration. The final experiment showed, firstly, that the failureto develop flavour aversions cannot be attributed to overshadowingby familiar visual cues and, secondly, that aversions for NaClflavoured food cannot be potentiated by the presence of a noveland highly salient visual cue. These results suggest that previousfailures to demonstrate flavoured food aversions in chicks arenot due to procedural inadequacies but, rather, due to an organismicconstraint. Whether this constraint is associative, physiologicalor attentional remains to be determined. The authors express appreciation to Marion Connors, Paula Halland Graeme Negri for technical assistance.     

Niche relations among three sympatric Mediterranean carnivores

Previous studies carried out in the Doñana National Park reported that red foxes (Vulpes vulpes) were killed by Iberian lynxes (Lynx pardinus), whereas similar-sized Eurasian badgers (Meles meles) were not. Therefore, we predicted that fox would avoid lynx predation risk by niche segregation whereas we did not expect such a segregation between badger and lynx. As an approach for evaluating our predictions, we compared their diet, activity patterns, and habitat use in an area of Doñana where the three carnivores are sympatric. Lynxes preyed almost uniquely on European rabbits (Oryctolagus cuniculus), and though badgers and foxes were omnivorous, rabbits also were a major prey, resulting in high overlaps throughout the year. However, badgers preyed largely on small rabbits, whereas lynxes and foxes preyed mainly on medium-sized rabbits. There were also interspecific differences in activity patterns. Maximum levels of activity among lynxes were during sunrise and dusk (49–67%). Foxes were most active during dusk and night (34–67%), and badgers were mainly nocturnal (53–87%). Though there were seasonal differences in the amount of activity of each species, specific activity patterns changed little throughout the year. There was a strong difference in annual habitat use by the three species (P?MAX) and the resting (P_MIN) periods. During P_MIN, foxes used the Mediterranean scrubland intensively (40% of locations on average), but during P_MAX, they used the pastureland much more intensively despite this habitat being poorer in their main prey (rabbits). As a consequence, foxes and lynxes exhibited segregation in their habitat use during the active period. Badgers also used the Mediterranean scrubland intensively, especially during P_MIN. There were no seasonal differences in habitat use for lynx and fox, but there was for badgers (P?相似文献   

The diet of Indian foxes in a peri-urban area of eastern India

Urban expansions into natural habitats have forced many carnivores to adapt to the modified areas; however, our understanding of their ecology in such areas is limited. The Indian fox (Vulpes bengalensis) is a small carnivore species that can adapt and exploit urban areas due to its generalist nature, but there is a paucity of data on Indian foxes in these human-modified areas. To understand the resource requirement of Indian foxes in urban habitats, we conducted a diet analysis by examining 119 scats of Indian foxes in a peri-urban habitat of Baripada town, Odisha, eastern India. To determine the diet composition of Indian foxes, we analyzed scat contents by their frequency occurrence (%FO), the relative frequency of occurrence (%RF) and mean percent volume (%Vm). Indian foxes consumed a wide range of food categories, including arthropods, rodents, reptiles, birds, plant parts and anthropogenic resources. In %Vm, rodents showed the highest volume, followed by polythene, Spondias pinnata fruit and Coleoptera. We found anthropogenic foods in considerable quantities, including polythene and paper. The diet of Indian foxes indicates that the species has opportunistic and generalist feeding habits consisting primarily of easily accessible foods. Furthermore, management efforts should focus on the proper management of waste and control of anthropogenic food sources in urban habitats.     

Intergenerational incest aversion: self-reported sexual arousal and disgust to hypothetical sexual contact with family members

The biological costs of inbreeding are expected to have shaped human incest aversion. These costs depend on biological sex, relatedness, and age. Whereas previous studies have focused on investigating how these factors modulate incest aversion in siblings and cousins—family members of the same generation— we examined relatives of different generations. In a population-based sample, 2499 respondents reported reactions to imagined sexual behaviors with either a biological child or parent, a niece/nephew or aunt/uncle, or a stepchild or stepparent; these responses were compared to reactions to imagined sexual behaviors involving a friend's child or parent. Replicating prior results, women report stronger incest aversions than do men. We extend previous findings by showing that incest aversions tended to be stronger between close (vs. more distant) intergenerational relatives. Indeed, for biological relatives, decreased degree of relatedness was associated with decreased incest aversion, and for biological relatives, the certainty in relatedness was also positively associated with incest aversion. As expected, age modulated sexual aversion for unrelated, but not related, target individuals. Sexual aversions towards step-relatives did not differ from sexual aversions to biological relatives.     

Taste aversion learning and aging: a comparison with the effect of dorsal hippocampal lesions in rats

The relationship between hippocampal function and aging was explored in Wistar rats using taste aversion learning by comparing the performance of adult dorsal hippocampal lesioned and fifteen-month-old intact rats with that of adult intact rats. In experiment 1 the conditioned blocking phenomenon was absent in the hippocampal and the aging rats. Unlike the adult intact rats, the hippocampal and aging rats were not impaired in acquiring a learned aversion to a cider vinegar solution (3 %) presented as a serial compound with a previously conditioned saccharin solution (0.1 %). In experiment 2 both the hippocampal and the aging rats developed reduced aversions to a saline solution (0.5 %) followed by an i.p. injection of lithium chloride (0.15 M; 2 % b.w.) if the taste solution was previously preexposed without consequences. This latent inhibition effect was similar to that seen in intact adult rats. In both experiments, the aging rats exhibited enhanced conventional learned taste aversions. It is concluded that aging is not a unitary process but induces both hippocampal dependent and hippocampal independent complex changes in the functioning of the neural circuits, implementing taste aversion learning.     

Evaluating seasonal bait delivery to badgers using rhodamine B

In the UK and Ireland, research on the control of bovine tuberculosis in badgers includes the development of a palatable bait for oral delivery of a vaccine and a means of its deployment in the field. In the present study, we carried out field deployment of bait according to the established method of bait marking in early spring and early summer to compare the effects of seasonality on bait uptake rates. All baits contained rhodamine B (RhB) which was subsequently detected in the hair and whiskers of captured badgers. During the 8 days of bait feeding at 14 badger setts, 99% of baits deployed in spring, and 100% of those deployed in summer were removed. The presence of RhB in captured badgers indicated high rates of uptake amongst adult badgers in spring (93%) and summer (98%). Only cubs captured in summer showed evidence of having taken bait (91%). Between 67% and 100% of each social group was estimated to have taken bait. The detection of RhB in 96% of badgers captured at outlier setts, where bait was not fed, suggested that deployment at main setts alone may be sufficient to target a relatively high proportion of the badger population. The number of baits deployed per marked badger suggested that a similar level of uptake might be achievable using fewer baits. The results clearly demonstrate the potential value of the bait-marking methodology for delivering vaccine baits to badgers during spring and summer, but that deployment in early summer is necessary to target cubs.     

Plasticity of olfactory orientation to foods in the snailAchatina fulica

Summary Snails were tested in an olfactometer for their orientation to food odours. Measures of odour choice, latency to make a choice and percentage of upwind orientations were obtained after experimental manipulations of dietary experience and hunger motivation. Juvenile snails, given an exclusive diet of a certain food for 12 h or less, oriented preferentially toward the odour of that food when subsequently presented with a choice between it and a novel food odour (Fig. 2). A 48 h period of exposure to a food resulted in a 21 day retention of the odour preference (Fig. 3). There was no evidence for an especially sensitive period for conditioning during the first 50 days of age (Fig. 4); however, adult snails (minimum 1 year old) required longer periods of dietary exposure to establish equivalent food odour memories (Fig. 5). Measures of latency and percentage of upwind orientations confirmed the choice data in demonstrating an effect of dietary experiences on olfactory orientation. Hunger motivation increased the selection for familiar food odours, and reduced the latency (Fig. 6 and Tables 3 and 4). Sensory adaptation appears inadequate to explain the conditioning phenomenon since formation of the preferences was contingent upon ingestion of the foods; exposure to the food odours alone was insufficient (Table 2). The data suggest that orientation preferences derive from a learned association between the odour of a food and its nutritional value.We thank Dr. Donald Kramer for helpful criticism throughout the course of this work. The research was supported financially by the National Research Council of Canada and le Ministère de l'Education du Québec.     

Estradiol benzoate can function as an unconditioned stimulus in a conditioned taste aversion paradigm

The extent to which gonadal steroid hormones can serve as unconditioned stimuli in a conditioned taste aversion paradigm was examined in Rockland-Swiss albino mice. With saccharin serving as the conditioned stimulus, subcutaneously injected estradiol benzoate, but not progesterone or testosterone propionate, was found to be a potent unconditioned stimulus in both male and female mice. Dose-response effects were also observed; increasing dosages of estradiol benzoate led to increasingly stronger conditioned aversions in both males and females. The aversion detected in males was more resistant to extinction than that seen in females. Prepubertal gonadectomy reversed the sex-dependent effects of estradiol benzoate in learned aversions in adulthood; castration of males promoted the extinction process, whereas ovariectomy of females retarded extinction. The results may be useful for our understanding of the mechanisms involved in conditioned taste aversion learning as well as a wide array of hormone-dependent behavioral responses.