School for Skinks: Can Conditioned Taste Aversion Enable Bluetongue Lizards (Tiliqua scincoides) to Avoid Toxic Cane Toads (Rhinella marina) as Prey?

The invasion of cane toads (Rhinella marina) through Australia imperils native predators that are killed if they consume these toxic anurans. The magnitude of impact depends upon the predators’ capacity for aversion learning: toad impact is lower if predators can learn not to attack toads. In laboratory trials, we assessed whether bluetongue lizards (Tiliqua scincoides) – a species under severe threat from toads – are capable of learned taste aversion and whether we can facilitate that learning by exposing lizards to toad tissue combined with a nausea‐inducing chemical (lithium chloride). Captive bluetongues rapidly learned to avoid the ‘unpalatable’ food. Taste aversion also developed (albeit less strongly) in response to meals of minced cane toad alone. Our data suggest that taste aversion learning may help bluetongue lizards survive the onslaught of cane toads, but that many encounters will be fatal because the toxin content of toads is so high relative to lizard tolerance of those toxins. Thus, baiting with nausea‐inducing (but non‐lethal) toad products might provide a feasible management option to reduce the impact of cane toad invasion on these native predators.     

A Behavioral Mechanism for Incorporating an Unpalatable Food in the Diet of a Generalist Herbivore (Orthoptera: Acrididae)

We investigated mechanisms that could lead to incorporation of unpalatable foods into the diet of a generalist grasshopper, Schistocerca americana: nutritional stress, habituation, learning, and attraction to novelty. The model system involved mesquite, a palatable but inferior food, and mulberry, an unpalatable but adequate food. Nutritional stress, due to prolonged intake of the inferior food, mesquite, did not increase the acceptability of mulberry. Habituation to the deterrent compounds in mulberry and associative learning of the nutritional benefits of mulberry also did not occur. However, mulberry became more acceptable after a day of restriction to a single food type other than mulberry, and even deterrent and nutritionally worthless alternatives such as filter paper became acceptable after a day on any one food type. A tendency to feed on novel food types may be a proximate mechanism for the incorporation of relatively unpalatable, but nutritionally valuable foods into the diet. Novelty and the apparent need for diversity of foods are discussed in the context of exploratory foraging behavior by generalist herbivores.     

Neuropeptides and amphibian prey-catching behavior

In mammals, a number of hypothalamic neuropeptides have been implicated in stress-induced feeding disorders. Recent studies in anurans suggest that stress-related neuropeptides may act on elemental aspects of visuomotor control to regulate feeding. Corticotropin-releasing hormone (CRH) and alpha-melanocyte-stimulating hormone, potent an orexic peptides in mammals, inhibit visually-guided prey-catching in toads. Neuropeptide Y (NPY), an orexic peptide in mammals, may be an important neuromodulator in inhibitory pre-tectal-tectal pathways involved in distinguishing predator and prey. Melanocortin, NPY and CRH neurons project onto key visuomotor structures within the amphibian brain, suggesting physiological roles in the modulation of prey-catching. Thus, neuropeptides involved in feeding behavior in mammals influence the efficacy of a visual stimulus in releasing prey-catching behavior. These neuropeptides may play an important role in how frogs and toads gather and process visual information, particularly during stress.     

Drosophila rely on learning while foraging under semi‐natural conditions

Learning is predicted to affect manifold ecological and evolutionary processes, but the extent to which animals rely on learning in nature remains poorly known, especially for short‐lived non‐social invertebrates. This is in particular the case for Drosophila, a favourite laboratory system to study molecular mechanisms of learning. Here we tested whether Drosophila melanogaster use learned information to choose food while free‐flying in a large greenhouse emulating the natural environment. In a series of experiments flies were first given an opportunity to learn which of two food odours was associated with good versus unpalatable taste; subsequently, their preference for the two odours was assessed with olfactory traps set up in the greenhouse. Flies that had experienced palatable apple‐flavoured food and unpalatable orange‐flavoured food were more likely to be attracted to the odour of apple than flies with the opposite experience. This was true both when the flies first learned in the laboratory and were then released and recaptured in the greenhouse, and when the learning occurred under free‐flying conditions in the greenhouse. Furthermore, flies retained the memory of their experience while exploring the greenhouse overnight in the absence of focal odours, pointing to the involvement of consolidated memory. These results support the notion that even small, short lived insects which are not central‐place foragers make use of learned cues in their natural environments.     

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.     

Patterns of chemical defense among Caribbean gorgonian corals: a preliminary survey

Ship-board assays employing the common Caribbean wrasse Thalassoma bifasdatum (Bloch) were undertaken to determine the palatability of food pellets coated with freshly-extracted, lipid-soluble metabolites of 37 types of Caribbean gorgonian corals representing at least 19 species from 11 genera. Extracts of 19 types (51%) were highly unpalatable (zero or one of five pellets eaten), four types (11%) were moderately unpalatable (two or three of five pellets eaten) and 14 (38%) were palatable (four or five of five pellets eaten) to fish in feeding assays. Gorgonians of the genera Pterogorgia (three types) and Eunicea (nine types) were consistently highly unpalatable, those of the genus Plexaurella (four types) were palatable and those of the genus Plexaura were most frequently palatable (six of eight types). Further assays of serial dilutions of extracts from seven representative, unpalatable types revealed that extracts inhibited fish feeding at pellet concentrations near or below the concentrations that metabolites occur in the gorgonian soft tissue. Extracts of Erythropodium caribaeorum (Duchassaing and Michelotti) and Pseudopterogorgia rigida (Bielschowsky) deterred fish feeding at pellet concentrations less than an order of magnitude lower than those found in the soft tissues of the corresponding gorgonians. Thin layer chromatographic analyses of extracts revealed the presence of lipid-soluble, secondary metabolites in a majority of the highly unpalatable extracts, although secondary metabolites were also present in a smaller percentage of palatable extracts. These data support the hypothesis that the soft tissues of many gorgonian corals contain lipid-soluble feeding deterrents which act as a defense against predation.     

Temporal discharge patterns of tectal and medullary neurons chronically recorded during snapping toward prey in toads Bufo bufo spinosus

In freely moving toads, the temporal discharge patterns of tectal and medullary neurons were observed during prey-catching.

1. Tectal T5.2 and T8.1 neurons displayed a premotor warming up firing that in the former was addressed specifically to prey orienting or snapping and in the latter generally to almost any kind of body movement.
2. The temporal discharge patterns of T5.2 neurons during snapping were different from those during orienting toward prey. Snapping started in the peak phase of warming up; firing was immediately terminated during the snap; thereafter some rebound activity was observed. Orienting started after the premotor warming up in the declining phase whilst the neuron kept on firing during orienting and then settled when the orienting movement was completed.
3. In toads which were not motivated to catch prey — comparabl to immobilized ones — the discharge frequency of T5.2 neurons toward a prey stimulus revealed no such warming up.
4. Because it is known that prey-selective T5.2 neurons are controlled by pretectal inhibitory influences, the following experiment was conducted: during recording a T5.2 neuron a pretectal lesion was applied ipsilaterally to the recording site. After a few seconds, the neuron showed a strong premotor wanning up in response to any kind of moving object, followed by prey-catching.
5. In the medulla oblongata, different H-type neurons of the hypoglossal nucleus displayed specific discharge patterns which resembled the tongue protractor and retractor muscle activities; a third type resembled the activity of the genio/sterno-hyoid muscle, which are suggested to stabilize the hyoid bone during snapping.
6. There were medullary M8-type neurons with properties similar to T8.1.
7. Snapping could be triggered by electrical stimulation of the optic tectum in the representation of the frontal visual field, but not by stimulation in the hypoglossal nucleus or the adjacent medial reticular formation.
8. A concept of a neuronal circuit for the coordination of tongue muscle contractions in response to prey is proposed.

     

Risky Courtship: Background Contrast,Ornamentation, and Display Behavior of Wolf Spiders Affect Visual Detection by Toad Predators

Males that search widely for females and perform conspicuous courtship displays run a high risk of being detected by their predators. Therefore, gains in reproductive success might be offset by increased mortality due to predation. Male brush‐legged wolf spiders (Schizocosa ocreata) with larger decorative traits (foreleg tufts) are preferred by females as mates, but are more readily detected by predators. However, predation risk may also be influenced by the interaction between components of signals and the environment in which signaling occurs. Courting male spiders were readily accepted as prey by a sympatric predator, the American toad (Anaxyrus americanus). We used video playback to tease apart the interactive effect between visual signals and the signaling environment on the ability of toads to detect courting spiders as a function of distance, background contrast, the presence or absence of male foreleg tufts, and behavioral activity. The response of toads to video sequences of male spiders was similar to their response to live male spiders. Toad response varied over distance toward spiders displayed against high contrast (sunny) vs. low contrast (shaded) backgrounds. Beyond 30 cm, more toads detected courting male spiders against light, ‘sunny’ backgrounds and detected them faster when compared to the same spider stimulus against darker, ‘shady’ backgrounds. In choice tests, toads oriented more often toward courting males with leg tufts than those without. Toad responses also varied with male spider behavior in that only videos of moving males were attacked. Latency to orient and detection by toads was significantly greater for walking males than courting males, and this effect was most evident at distances between 30 cm and 50 cm. Results supported that courting wolf spiders are at significant risk of predation by visually acute predators. Distance, background contrast, and the presence of foreleg decorations influence detection probability. Thus, the same complex visual signals that make males conspicuous and are preferred by females can make males more vulnerable as prey to toads.     

Invasive Cane Toads: Social Facilitation Depends upon an Individual’s Personality

Individual variation in behavioural traits (including responses to social cues) may influence the success of invasive populations. We studied the relationship between sociality and personality in invasive cane toads (Rhinella marina) from a recently established population in tropical Australia. In our field experiments, we manipulated social cues (the presence of a feeding conspecific) near a food source. We captured and compared toads that only approached feeding sites where another toad was already present, with conspecifics that approached unoccupied feeding sites. Subsequent laboratory trials showed correlated personality differences (behavioural syndromes) between these two groups of toads. For example, toads that approached already-occupied rather than unoccupied feeding sites in the field, took longer to emerge from a shelter-site in standardized trials, suggesting these individuals are ‘shy’ (whereas toads that approached unoccupied feeding stations tended to be ‘bold’). Manipulating hunger levels did not abolish this difference. In feeding trials, a bold toad typically outcompeted a shy toad under conditions of low prey availability, but the outcome was reversed when multiple prey items were present. Thus, both personality types may be favored under different circumstances. This invasive population of toads contains individuals that exhibit a range of personalities, hinting at the existence of a wide range of social dynamics in taxa traditionally considered to be asocial.     

Configurational prey-selection by individual experience in the toadBufo bufo

Summary The habituation method was used to investigate the toad's ability to discriminate between two dimensional prey dummies of different shapes and patterns: If immediately following habituation of the prey-catching orienting behavior to a dummy form A, prey-catching responses are elicited when another form B is presented, it can be concluded that the toad is able to discriminate between the two patterns. The results show that toads are able to discern detailed structures within the outline limits of a 5 mm× 20 mm worm-like shape, on the basis of individual experience (stimulus specific habituation). In particular the results demonstrate that triangular stimulus patterns moved with a horizontal acute angle leading increase the releasing value of prey features whereas separate additional dots moved simultaneously may reduce the prey features of an optimal prey dummy. Dots, stripes and acute angles obviously have a significant effect in theexperience governed pattern discrimination of prey for toadsBufo bufo.Supported by grants of the Deutsche Forschungsgemeinschaft Ew 7/6     

Brittle-star bioluminescence functions as an aposematic signal to deter crustacean predators

The behaviour of three species of nocturnally active, visually orienting crabs (Portunus sebae, P. spinnimanus and P. ordwayi) was observed to determine whether the luminescent signals produced by Ophiopsila riisei (Echinodermata: Ophiuroidea) function as an aposematic deterrent against crustacean predators. In repeated experimental trials, crabs showed more rapid rejection of luminescent unpalatable ophiuroids than of non-luminescent controls. After five trials, unpalatable luminescent prey were rejected three times as quickly as either unpalatable or palatable non-luminescent controls. Over the course of the trials, crabs damaged fewer luminescent ophiuroids than non-luminescent controls. Furthermore, blind crabs (that could not perceive the luminescent flashes) caused significantly more damage to luminescent brittle-stars than did crabs with intact eyes (that could see the light signals). All three species of crab ophiuroids versus non-luminescent controls. Ophiopsila riisei survived the majority of crab attacks, and crabs can therefore learn to reject unpalatable luminescent prey without killing them. This suggests that individual selection may be an important mechanism for the evolution of aposematic luminescent signals in this, and probably other, luminescent species.     

An evaluation of chemical and physical defenses against fish predation in a suite of seagrass-associated ascidians

The palatability of two solitary and three colonial species of ascidians commonly found in sub-tropical seagrass meadows was evaluated using the abundant, sympatric, omnivorous pinfish Lagodon rhomboides as a model predator. Bite-sized pieces of fresh tissues of both solitary and one of the three colonial ascidian species were unpalatable to fish. Lipophilic and hydrophilic extracts of the three unpalatable species did not cause feeding deterrence indicating that secondary metabolites are not responsible for the lack of palatability. Distaplia bermudensis, the one colonial ascidian that was unpalatable to fish, had a highly acidified outer tunic (pH = 1.5). We tested the ability of acidified agar food pellets (pH = 1.5) to deter pinfish and found that the fish readily ingested acidified pellets. The toughness of the tunic of all five ascidian species was evaluated by measuring the Force (N) required to penetrate the tunic using a penetrometer. Tunic toughness is likely to explain the lack of palatability of the solitary ascidians Styela plicata and Molgula occidentalis as their tunics required a force of > 34 N to penetrate. Tunic toughness may be a particularly effective adaptation for ascidian defense in seagrass habitats where fish with strong crushing jaws, such as those that commonly occur in coral reef systems, are rare.     

Adaptation or preadaptation: why are keelback snakes (<Emphasis Type="Italic">Tropidonophis mairii</Emphasis>) less vulnerable to invasive cane toads (<Emphasis Type="Italic">Bufo marinus</Emphasis>) than are other Australian snakes?

Biological invasions can expose native predators to novel prey which may be less nutritious or detrimental to predators. The introduction and subsequent spread of cane toads (Bufo marinus) through Australia has killed many anuran-eating snakes unable to survive the toad’s toxins. However, one native species, the keelback snake (Tropidonophis mairii), is relatively resistant to toad toxins and remains common in toad-infested areas. Is the keelback’s ability to coexist with toads a function of its ancestral Asian origins, or a consequence of rapid adaptation since cane toads arrived in Australia? And does the snake’s feeding preference for frogs rather than toads reflect an innate or learned behaviour? We compared keelback populations long sympatric with toads with a population that has encountered toads only recently. Unlike toad-vulnerable snake species, sympatry with toads has not affected keelback toxin tolerances or feeding responses: T. mairii from toad-sympatric and toad-naïve populations show a similar sensitivity to toad toxin, and a similar innate preference for frogs rather than toads. Feeding responses of neonatal keelbacks demonstrate that learning plays little or no role in the snake’s aversion to toads. Thus, behavioural aversion to B. marinus as prey, and physiological tolerance to toad toxins are pre-existing innate characteristics of Australian keelbacks rather than adaptations to the cane toad’s invasion of Australia. Such traits were most likely inherited from ancestral keelbacks that adapted to the presence of bufonids in Asia. Our results suggest that the impact of invasive species on native taxa may be strongly influenced by the biogeographic histories of the species involved.     

Far from home: responses of an American predator species to an American prey species in a jointly invaded area of Australia

Far from their native ranges in the Americas, two invasive species come into contact in Australian waterbodies. Cane toads (Rhinella marina) fatally poison many anurophagous predators, whereas eastern mosquito fish (Gambusia holbrooki) voraciously consume anuran larvae. As cane toads spread south along Australia’s east coast, they are colonizing areas where mosquito fish are abundant. What happens when these two American invaders encounter each other in Australia? We tested the responses to toad tadpoles of mosquito fish from populations that were sympatric versus allopatric with cane toads. Toad-sympatric fish generally ignored toad tadpoles. Toad-allopatric fish initially consumed a few tadpoles, but rapidly developed an aversion to these toxic prey items. The laboratory-reared progeny of toad-allopatric fishes were more likely to approach toad tadpoles than were the offspring of toad-sympatric fishes, but the two groups learned toad-avoidance at similar rates. Thus, mosquito fish show an innate aversion to cane toad tadpoles (perhaps reflecting coevolution with North American bufonid taxa), as well as an ability to rapidly learn taste-aversion. Our comparisons among populations suggest that several decades of toad-free existence in Australia caused a decline in the fishes’ innate (heritable) aversion to toads, but did not affect the fishes’ capacity to learn toad-avoidance after an initial exposure. Any impact of mosquito fish on cane toads thus is likely to be transitory. The rapid (<100-year) time frame of these shifts (the initial weakening of the fishes’ response during toad-allopatry, and its recovery after secondary contact) emphasizes the dynamic nature of faunal responses during biological invasions, and the interplay between adaptation and phenotypic plasticity.     

Effects of prey quantity and quality on predatory wasps

1. The simultaneous effects of prey quantity and prey quality on fitness correlates of the predatory wasp Polistes fuscatus were examined in a glasshouse study. Prey quantity was manipulated by providing prey in excess (high quantity) or one‐third of that (low quantity). Prey quality was manipulated by providing either palatable (Manduca sexta) caterpillars or unpalatable (Junonia coenia) caterpillars. 2. The effect of prey quality on wasp production depended on prey quantity. Nests given unpalatable prey produced few wasps whereas nests given palatable prey increased wasp production with increased prey. 3. The low production of nests given unpalatable prey reflected the low acceptability of those prey. The wasps preferred the palatable prey and learned to reject the unpalatable prey. With no choice of prey, they took only enough unpalatable prey to develop a small nest or colony. 4. A diet of unpalatable prey also resulted in smaller wasps and reduced the proportion of males produced, from about 40% to just 8–14%, depending on the year.     

The impact of food type, temperature and starvation on larval development of Balanus amphitrite Darwin (Cirripedia: Thoracica)

The impact of diatom food species (Chaetoceros calcitrans and Skeletonema costatum), temperature and starvation on the larval development of Balanus amphitrite was evaluated. Starvation threshold levels for different ages of larvae (0- to 5-day-old) fed with C. calcitrans and S. costatum and then starved at 5, 15 and 25 °C temperature were estimated as ultimate recovery hour (URH; denoting the starvation point in hours at the end of which larvae can recover and continue development). Effect of temperature on starvation threshold varied significantly with larval age and food species. The URH declined with larval age at 5 °C, but not at 15 and 25 °C. The URH and grazing rates were high for early instars fed on C. calcitrans, and for advanced instars fed on S. costatum. Carbon gain through feeding was maximum for 2-day-old larvae when fed with C. calcitrans and decreased with larval age. However, when fed with S. costatum carbon gain increased with larval age. This confirms that with development the utility of food types changes. The differences in the carbon gain can be attributed to differences in grazing rate due to variations in the size of the diatom cells, larval intersetular distance, diatom sinking rate and the photo-taxic behavior of larvae. Molting was observed at times when larvae were undergoing starvation and this could be viewed as stress-induced molting, and it differed with the larval age and food organisms.     

A neural model of interactions subserving prey-predator discrimination and size preference in anuran amphibia

The model described is an extension of a previous model of the optic tectum (Arbib & Lara, 1982; Lara, Arbib & Cromarty, 1982; Lara & Arbib, 1982) and takes into consideration anatomical, physiological and behavioral studies in anurans, as well as earlier modelling efforts (Ewert & Von Seelen, 1974; Didday, 1976). Computer simulations were conducted to analyze how interactions among retina, optic tectum and pretectum may give frogs and toads the ability to discriminate between prey and predator stimuli. Results from simulations have allowed us to reproduce empirical observations, to suggest new experiments, and to postulate what neural mechanisms might be involved in some phenomena related to prey-catching orienting behavior, with direction invariance of prey-predator recognition being a consequence of tectal architecture, and size preference and response latency depending on the motivational state of the animal.     

Testing chemical defence based on pyrrolizidine alkaloids

Pyrrolizidine alkaloids are considered the primary defence mechanism in aposematic ithomiine butterflies and arctiid moths. Despite evidence that pyrrolizidine alkaloids are effective against some invertebrate predators, proof for a protective function of pyrrolizidine alkaloids against vertebrate predators is fragmented. The present work shows that the pyrrolizidine alkaloid monocrot-aline is unpalatable to the pileated finch,Coryphospingus pileatusand that the unpalatability is learned through association with a specific colour pattern (blue stripes). In a series of trials, using mealworms as model prey, birds rejected those to which pyrrolizidine alkaloid solution had been applied topically but accepted prey devoid of the alkaloid. Subsequent offerings of prey with pyrrolizidine alkaloid and a painted blue-striped pattern led to consistent rejections by the experimental birds. Birds were then offered blue-striped painted larvae without pyrrolizidine alkaloids (‘mimics’), which were rejected at levels similar to the previous trial. The predators learned to recognize the prey as unpalatable items based on their experience in the previous encounters. These results provide evidence for the protective capacity of the pyrrolizidine alkaloid against a vertebrate predator and supports the role of these chemicals in aposematism in the Lepidoptera.     

Stress, neuropeptides, and feeding behavior: a comparative perspective

Stress inhibits feeding behavior in all vertebrates. Data frommammals suggest an important role for hypothalamic neuropeptides,in particular the melanocortins and corticotropin-releasinghormone (CRH)-like peptides, in mediating stress-induced inhibitionof feeding. The effects of CRH on food intake are evolutionarilyancient, as this peptide inhibits feeding in fishes, birds,and mammals. The effects of melanocortins on food intake havenot been as extensively studied, but available evidence suggeststhat the anorexic role of neuronal melanocortins has been conserved.Although there is evidence that CRH and the melanocortins influencehypothalamic circuitry controlling food intake, these peptidesmay have a more primitive role in modulating visuomotor pathwaysinvolved in the recognition and acquisition of food. Stressrapidly reduces visually guided prey-catching behavior in toads,an effect that can be mimicked by administration of CRH, whilecorticosterone and isoproterenol are without effect. Melanocortinsalso reduce prey-oriented turning movements and, in addition,facilitate the acquisition of habituation to a moving prey item.The effects of these neuropeptides are rapid, occurring within30 min after administration. Thus, changes in neuroendocrinestatus during stress may dramatically influence the efficacywith which visual stimuli release feeding behavior. By modulatingvisuomotor processing these neuropeptides may help animals makeappropriate behavioral decisions during stress.     

Effects of angiotensin II and bladder condition on hydration behavior and water uptake in the toad,Bufo woodhousei

• 1.1. Water absorption response (WR) behavior and water weight gain were examined in hydrated toads, Bufo woodhousei, treated with angiotensin II (All) or with a control Ringer's solution. The effects of urinary bladder condition (ad lib. bladder urine or empty bladder) were examined concurrently.
• 2.2. Toads treated with All (100μg/100g body weight), spent more time in WR posture and absorbed more water than Ringer's-injected toads.
• 3.3. Toads with empty bladders maintained WR posture for longer periods of time and gained more weight than toads whose bladders were not emptied.
• 4.4. The effects of All and bladder urine on water absorption by B. woodhousei appear to be separate and additive.