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    ABSTRACT: Avian predators readily learn to associate the warning coloration of aposematic prey with the toxic effects of ingesting them, but they do not necessarily exclude aposematic prey from their diets. By eating aposematic prey 'educated' predators are thought to be trading-off the benefits of gaining nutrients with the costs of eating toxins. However, while we know that the toxin content of aposematic prey affects the foraging decisions made by avian predators, the extent to which the nutritional content of toxic prey affects predators' decisions to eat them remains to be tested. Here, we show that European starlings (Sturnus vulgaris) increase their intake of a toxic prey type when the nutritional content is artificially increased, and decrease their intake when nutritional enrichment is ceased. This clearly demonstrates that birds can detect the nutritional content of toxic prey by post-ingestive feedback, and use this information in their foraging decisions, raising new perspectives on the evolution of prey defences. Nutritional differences between individuals could result in equally toxic prey being unequally predated, and might explain why some species undergo ontogenetic shifts in defence strategies. Furthermore, the nutritional value of prey will likely have a significant impact on the evolutionary dynamics of mimicry systems.
    Proceedings of the Royal Society B: Biological Sciences 02/2014; 281(1781):20133255. DOI:10.1098/rspb.2013.3255
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    ABSTRACT: Artificial grammars (AG) are designed to emulate aspects of the structure of language, and AG learning (AGL) paradigms can be used to study the extent of nonhuman animals' structure-learning capabilities. However, different AG structures have been used with nonhuman animals and are difficult to compare across studies and species. We developed a simple quantitative parameter space, which we used to summarize previous nonhuman animal AGL results. This was used to highlight an under-studied AG with a forward-branching structure, designed to model certain aspects of the nondeterministic nature of word transitions in natural language and animal song. We tested whether two monkey species could learn aspects of this auditory AG. After habituating the monkeys to the AG, analysis of video recordings showed that common marmosets (New World monkeys) differentiated between well formed, correct testing sequences and those violating the AG structure based primarily on simple learning strategies. By comparison, Rhesus macaques (Old World monkeys) showed evidence for deeper levels of AGL. A novel eye-tracking approach confirmed this result in the macaques and demonstrated evidence for more complex AGL. This study provides evidence for a previously unknown level of AGL complexity in Old World monkeys that seems less evident in New World monkeys, which are more distant evolutionary relatives to humans. The findings allow for the development of both marmosets and macaques as neurobiological model systems to study different aspects of AGL at the neuronal level.
    The Journal of Neuroscience : The Official Journal of the Society for Neuroscience 11/2013; 33(48):18825-18835. DOI:10.1523/JNEUROSCI.2414-13.2013
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    ABSTRACT: Predators that have learned to associate warning coloration with toxicity often continue to include aposematic prey in their diet in order to gain the nutrients and energy that they contain. As body size is widely reported to correlate with energetic content, we predicted that prey size would affect predators' decisions to eat aposematic prey. We used a well-established system of wild-caught European starlings, Sturnus vulgaris, foraging on mealworms, Tenebrio molitor, to test how the size of undefended (water-injected) and defended (quinine-injected) prey, on different coloured backgrounds, affected birds' decisions to eat defended prey. We found that birds ate fewer defended prey, and less quinine, when undefended prey were large compared with when they were small, but that the size of the defended prey had no effect on the numbers eaten. Consequently, we found no evidence that the mass of the defended prey or the overall mass of prey ingested affected the amount of toxin that a predator was willing to ingest, and instead the mass of undefended prey eaten was more important. This is a surprising finding, challenging the assumptions of state-dependent models of aposematism and mimicry, and highlighting the need to understand better the mechanisms of predator decision making. In addition, the birds did not learn to discriminate visually between defended and undefended prey based on size, but only on the basis of colour. This suggests that colour signals may be more salient to predators than size differences, allowing Batesian mimics to benefit from aposematic models even when they differ in size.
    Animal Behaviour 06/2013; 85(6):1315-1321. DOI:10.1016/j.anbehav.2013.03.021
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    ABSTRACT: Toxic prey species living in the same environment have long been thought to mutually benefit from having the same warning signal by sharing the education of naïve predators. In contrast, 'saturation theory' predicts that predators are physiologically limited by the amount of toxin that they can eat in a given time period. Therefore, sympatric species that contain the same toxin should mutually benefit from reduced predation even when they are visually distinct, reducing the benefits to visual mimicry. For the first time, we found that mutualism can occur between unequally defended prey that are visually distinct, although the benefits to each prey type depends on the predators' abilities and/or motivation to visually discriminate between them. Furthermore, we found that this variability in predatory behaviour had a significant impact on the benefits of mimicry for unequally defended prey. Our results demonstrate that variability in the foraging decisions of predators can have a significant effect on the benefits of shared toxicity and visual mimicry between sympatric species, and highlights the need to consider how predators exert selection pressures on models and mimics over their entire lifetimes.
    PLoS ONE 09/2012; 7(9):e44895. DOI:10.1371/journal.pone.0044895
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    ABSTRACT: Laboratory studies have shown that images of eyes can cause people to behave more cooperatively in some economic games, and in a previous experiment, we found that eye images increased the level of contributions to an honesty box. However, the generality and robustness of the eyes effect is not known. Here, we extended our research on the effects of eye images on cooperative behavior to a novel context—littering behavior in a university cafeteria—and attempted to elucidate the mechanism by which they work, by displaying them both in conjunction with, and not associated with, verbal messages to clear one's litter. We found a halving of the odds of littering in the presence of posters featuring eyes, as compared to posters featuring flowers. This effect was independent of whether the poster exhorted litter clearing or contained an unrelated message, suggesting that the effect of eye images cannot be explained by their drawing attention to verbal instructions. There was some support for the hypothesis that eye images had a larger effect when there were few people in the café than when the café was busy. Our results confirm that the effects of subtle cues of observation on cooperative behavior can be large in certain real-world contexts.
    Evolution and Human Behavior 05/2011; 32(3). DOI:10.1016/j.evolhumbehav.2010.10.006
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    ABSTRACT: The evolution and maintenance of toxicity in a prey population is a challenge to evolutionary biologists if the investment in toxin does not benefit the individual. Recent experiments suggest that taste-rejection behaviour enables predators to selectively ingest less toxic individuals, which could stabilize investment in defences. However, we currently do not know if taste rejection of defended prey is accurate across different contexts, and that prey always benefit according to their investment. Using avian predators, we show that the rejection probability does not solely depend on the investment in defence by an individual, but also on the investment by other individuals in the same population. Therefore, taste rejection by predators could lead to destabilization in the investment in defences, and allow variability in prey defences to exist.
    Biology letters 03/2010; 6(5):617-9. DOI:10.1098/rsbl.2010.0153
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    ABSTRACT: Many prey species have evolved bitter-tasting toxins that effectively protect them from potential predators. While predators can learn to associate the taste of defended prey with the noxious effects of the toxins, it is unclear whether bitter tastes also function as deterrents. We explicitly tested the effectiveness of a nontoxic distasteful chemical as an antipredator defence. We gave four groups of European starlings, Sturnus vulgaris, a sequential colour discrimination task, where one colour signalled undefended mealworms, Tenebrio molitor, and the other signalled defended mealworms that had either been injected with or coated with either a high or a low concentration of Bitrex solution (a nontoxic bitter-tasting solution). Birds ate all of the prey presented in this way, but performed disgust responses after eating prey coated in Bitrex solution. Birds were then given a series of trials in which they received defended and undefended prey items simultaneously. Birds that received prey injected with Bitrex attacked similar numbers of defended and undefended prey, whereas birds that received prey coated in Bitrex ate significantly fewer defended than undefended prey. Birds given prey coated in a high concentration of Bitrex showed a stronger preference for undefended prey than birds given prey coated in a low concentration of Bitrex. Our experiment demonstrates that a nontoxic distasteful chemical can protect insect prey from predation, but only under very specific conditions.
    Animal Behaviour 09/2009; 78(3-78):761-766. DOI:10.1016/j.anbehav.2009.07.006
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    ABSTRACT: Recent studies have provided a new perspective on the relationship between the honey bee queen and her colony. They suggest that the queen produces a pheromone which pharmacologically manipulates her workers.
    Current biology: CB 08/2009; 19(14):R547-8. DOI:10.1016/j.cub.2009.05.032
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    ABSTRACT: Plants produce flowers with complex visual and olfactory signals, but we know relatively little about the way that signals such as floral scents have evolved. One important factor that may direct the evolution of floral signals is a pollinator's ability to learn. When animals learn to associate two similar signals with different outcomes, biases in their responses to new signals can be formed. Here, we investigated whether or not pollinators develop learned biases towards floral scents that depend on nectar reward quality by training restrained honeybees to learn to associate two similar odour signals with different outcomes using a classical conditioning assay. Honeybees developed learned biases towards odours as a result of differential conditioning, and the extent to which an olfactory bias could be produced depended upon the difference in the quality of the nectar rewards experienced during conditioning. Our results suggest that differences in reward quality offered by flowers influence odour recognition by pollinators, which in turn could influence the evolution of floral scents in natural populations of co-flowering plants.
    Proceedings of the Royal Society B: Biological Sciences 05/2009; 276(1667):2597-604. DOI:10.1098/rspb.2009.0040
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    ABSTRACT: There has been considerable speculation about the adaptive significance of the human female orgasm, with one hypothesis being that it promotes differential affiliation or conception with high-quality males. We investigated the relationship between women's self-reported orgasm frequency and the characteristics of their partners in a large representative sample from the Chinese Health and Family Life Survey. We found that women report more frequent orgasms the higher their partner's income is. This result cannot be explained by possible confounds such as women's age, health, happiness, educational attainment, relationship duration, wealth difference between the partners, difference between the partners in educational attainment, and regional location. It appears consistent with the view that female orgasm has an evolved adaptive function.
    Evolution and Human Behavior 03/2009; 30(2):146-151. DOI:10.1016/j.evolhumbehav.2008.11.002
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