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1.  Reduced flocking by birds on islands with relaxed predation. 
Adaptive hypotheses for the evolution of flocking in birds have usually focused on predation avoidance or foraging enhancement. It still remains unclear to what extent each factor has contributed to the evolution of flocking. If predation avoidance were the sole factor involved, flocking should not be prevalent when predation is relaxed. I examined flocking tendencies along with mean and maximum flock size in species living on islands where predation risk is either absent or negligible and then compared these results with matched counterparts on the mainland. The dataset consisted of 46 pairs of species from 22 different islands across the world. The tendency to flock was retained on islands in most species, but in pairs with dissimilar flocking tendencies, island species were less likely to flock. Mean and maximum flock size were smaller on islands than on the mainland. Potential confounding factors such as population density, nest predation, habitat type, food type and body mass failed to account for the results. The results suggest that predation is a significant factor in the evolution of flocking in birds. Nevertheless, predation and other factors, such as foraging enhancement, probably act together to maintain the trait in most species.
doi:10.1098/rspb.2004.2703
PMCID: PMC1691692  PMID: 15293857
2.  Evolution of embryonic developmental period in the marine bird families Alcidae and Spheniscidae: roles for nutrition and predation? 
Background
Nutrition and predation have been considered two primary agents of selection important in the evolution of avian life history traits. The relative importance of these natural selective forces in the evolution of avian embryonic developmental period (EDP) remain poorly resolved, perhaps in part because research has tended to focus on a single, high taxonomic-level group of birds: Order Passeriformes. The marine bird families Alcidae (auks) and Spheniscidae (penguins) exhibit marked variation in EDP, as well as behavioural and ecological traits ultimately linked to EDP. Therefore, auks and penguins provide a unique opportunity to assess the natural selective basis of variation in a key life-history trait at a low taxonomic-level. We used phylogenetic comparative methods to investigate the relative importance of behavioural and ecological factors related to nutrition and predation in the evolution of avian EDP.
Results
Three behavioural and ecological variables related to nutrition and predation risk (i.e., clutch size, activity pattern, and nesting habits) were significant predictors of residual variation in auk and penguin EDP based on models predicting EDP from egg mass. Species with larger clutch sizes, diurnal activity patterns, and open nests had significantly shorter EDPs. Further, EDP was found to be longer among birds which forage in distant offshore waters, relative to those that foraged in near shore waters, in line with our predictions, but not significantly so.
Conclusion
Current debate has emphasized predation as the primary agent of selection driving avian life history diversification. Our results suggest that both nutrition and predation have been important selective forces in the evolution of auk and penguin EDP, and highlight the importance of considering these questions at lower taxonomic scales. We suggest that further comparative studies on lower taxonomic-level groups will continue to constructively inform the debate on evolutionary determinants of avian EDP, as well as other life history parameters.
doi:10.1186/1471-2148-10-179
PMCID: PMC2896374  PMID: 20546608
3.  Foraging Patch Selection in Winter: A Balance between Predation Risk and Thermoregulation Benefit 
PLoS ONE  2013;8(7):e68448.
In winter, foraging activity is intended to optimize food search while minimizing both thermoregulation costs and predation risk. Here we quantify the relative importance of thermoregulation and predation in foraging patch selection of woodland birds wintering in a Mediterranean montane forest. Specifically, we account for thermoregulation benefits related to temperature, and predation risk associated with both illumination of the feeding patch and distance to the nearest refuge provided by vegetation. We measured the amount of time that 38 marked individual birds belonging to five small passerine species spent foraging at artificial feeders. Feeders were located in forest patches that vary in distance to protective cover and exposure to sun radiation; temperature and illumination were registered locally by data loggers. Our results support the influence of both thermoregulation benefits and predation costs on feeding patch choice. The influence of distance to refuge (negative relationship) was nearly three times higher than that of temperature (positive relationship) in determining total foraging time spent at a patch. Light intensity had a negligible and no significant effect. This pattern was generalizable among species and individuals within species, and highlights the preponderance of latent predation risk over thermoregulation benefits on foraging decisions of birds wintering in temperate Mediterranean forests.
doi:10.1371/journal.pone.0068448
PMCID: PMC3709897  PMID: 23874632
4.  The Importance of Predation Risk and Missed Opportunity Costs for Context-Dependent Foraging Patterns 
PLoS ONE  2014;9(5):e94107.
Correct assessment of risks and costs of foraging is vital for the fitness of foragers. Foragers should avoid predation risk and balance missed opportunities. In risk-heterogeneous landscapes animals prefer safer locations over riskier, constituting a landscape of fear. Risk-uniform landscapes do not offer this choice, all locations are equally risky. Here we investigate the effects of predation risk in patches, travelling risk between patches, and missed social opportunities on foraging decisions in risk-uniform and risk-heterogeous landscapes. We investigated patch leaving decisions of 20 common voles (M. arvalis) in three experimental landscapes: safe risk-uniform, risky risk-uniform and risk-heterogeneous. We varied both the predation risk level and the predation risk distribution between two patches experimentally and in steps, assuming that our manipulation consequently yield different distributions and levels of risk while foraging, risk while travelling, and costs of missed, social opportunities (MSOCs). We measured mean GUDs (giving-up density of food left in the patch) for both patches as a measure of foraging gain, and delta GUD, the differences among patches, as a measure of the spatial distribution of foraging effort over a period of six hours. Distribution of foraging effort was most even in the safe risk-uniform landscapes and least even in the risk-heterogeneous landscape, with risky risk-uniform landscapes in between. Foraging gain was higher in the safe than in the two riskier landscapes (both uniform and heterogeneous). Results supported predictions for the effects of risk in foraging patches and while travelling between patches, however predictions for the effects of missed social opportunities were not met in this short term experiment. Thus, both travelling and foraging risk contribute to distinct patterns observable high risk, risk-uniform landscapes.
doi:10.1371/journal.pone.0094107
PMCID: PMC4014466  PMID: 24809666
5.  Group-foraging is not associated with longevity in North American birds 
Biology Letters  2009;6(1):42-44.
Group-foraging is common in many animal taxa and is thought to offer protection against predators and greater foraging efficiency. Such benefits may have driven evolutionary transitions from solitary to group-foraging. Greater protection against predators and greater access to resources should reduce extrinsic sources of mortality and thus select for higher longevity according to life-history theory. I assessed the association between group-foraging and longevity in a sample of 421 North American birds. Taking into account known correlates of longevity, such as age at first reproduction and body mass, foraging group size was not correlated with maximum longevity, with and without phylogenetic correction. However, longevity increased with body mass in non-passerine birds. The results suggest that the hypothesized changes in predation risk with group size may not correlate with mortality rate in foraging birds.
doi:10.1098/rsbl.2009.0691
PMCID: PMC2817272  PMID: 19776065
body mass; group size; foraging; independent contrasts; maximum longevity; passerine versus non-passerine bird
6.  Interspecific reciprocity explains mobbing behaviour of the breeding chaffinches, Fringilla coelebs. 
When prey animals discover a predator close by, they mob it while uttering characteristic sounds that attract other prey individuals to the vicinity. Mobbing causes a predator to vacate its immediate foraging area, which gives an opportunity for prey individuals to continue their interrupted daily activity. Besides the increased benefits, mobbing behaviour also has its costs owing to injuries or death. The initiator of mobbing may be at increased risk of predation by attracting the predator's attention, especially if not joined by other neighbouring prey individuals. Communities of breeding birds have always been considered as temporal aggregations. Since an altruist could not prevent cheaters from exploiting its altruism in an anonymous community, this excluded any possibility of explaining mobbing behaviour in terms of reciprocal altruism. However, sedentary birds may have become acquainted since the previous non-breeding season. Migrant birds, forming anonymous communities at the beginning of the breeding season, may also develop closer social ties during the course of the breeding season. We tested whether a male chaffinch, a migrant bird, would initiate active harassment of a predator both at the beginning of the breeding season and a week later when it has become a member of a non-anonymous multi-species aggregation of sedentary birds. We expected that male chaffinches would be less likely to initiate a mob at the beginning of the breeding season when part of an anonymous multi-species aggregation of migratory birds. However, their mobbing activity should increase as the breeding season advances. Our results support these predictions. Cooperation among individuals belonging to different species in driving the predator away may be explained as interspecific reciprocity based on interspecific recognition and temporal stability of the breeding communities.
doi:10.1098/rspb.2002.2155
PMCID: PMC1691171  PMID: 12495502
7.  Predator experience on cryptic prey affects the survival of conspicuous aposematic prey. 
Initially, aposematism, which is an unprofitable trait, e.g. noxiousness conspicuously advertised to predators, appears to be a paradox since conspicuousness should increase predation by naive predators. However, reluctance of predators for eating novel prey (e.g. neophobia) might balance the initial predation caused by inexperienced predators. We tested the novelty effects on initial predation and avoidance learning in two separate conspicuousness levels of aposematic prey by using a 'novel world' method. Half of the wild great tits (Parus major) were trained to eat cryptic prey prior to the introduction of an aposematic prey, which potentially creates a bias against the aposematic morph. Both prey types were equally novel for control birds and they should not have shown any biased reluctance for eating an aposematic prey. Knowledge of cryptic prey reduced the expected initial mortality of the conspicuous morph to a random level whereas control birds initially ate the conspicuous morph according to the visibility risk. Birds learned to avoid conspicuous prey in both treatments but knowledge of cryptic prey did not increase the rate of avoidance learning. Predators' knowledge of cryptic prey did not reduce the predation of the less conspicuous aposematic prey and additionally predators did not learn to avoid the less conspicuous prey. These results indicate that predator psychology, which was shown as reluctance for attacking novel conspicuous prey, might have been important in the evolution of aposematism.
doi:10.1098/rspb.2000.1377
PMCID: PMC1088614  PMID: 11270431
8.  A Meta-Analysis of Predation Risk Effects on Pollinator Behaviour 
PLoS ONE  2011;6(6):e20689.
Flower-visiting animals are constantly under predation risk when foraging and hence might be expected to evolve behavioural adaptations to avoid predators. We reviewed the available published and unpublished data to assess the overall effects of predators on pollinator behaviour and to examine sources of variation in these effects. The results of our meta-analysis showed that predation risk significantly decreased flower visitation rates (by 36%) and time spent on flowers (by 51%) by pollinators. The strength of the predator effects depended neither on predator taxa and foraging mode (sit-and-wait or active hunters) nor on pollinator lifestyle (social vs. solitary). However, predator effects differed among pollinator taxa: predator presence reduced flower visitation rates and time spent on flowers by Squamata, Lepidoptera and Hymenoptera, but not by Diptera. Furthermore, larger pollinators showed weaker responses to predation risk, probably because they are more difficult to capture. Presence of live crab spiders on flowers had weaker effects on pollinator behaviour than presence of dead or artificial crab spiders or other objects (e.g. dead bees, spheres), suggesting that predator crypsis may be effective to some extent. These results add to a growing consensus on the importance of considering both predator and pollinator characteristics from a community perspective.
doi:10.1371/journal.pone.0020689
PMCID: PMC3113803  PMID: 21695187
9.  Group Dynamics of Zebra and Wildebeest in a Woodland Savanna: Effects of Predation Risk and Habitat Density 
PLoS ONE  2010;5(9):e12758.
Background
Group dynamics of gregarious ungulates in the grasslands of the African savanna have been well studied, but the trade-offs that affect grouping of these ungulates in woodland habitats or dense vegetation are less well understood. We examined the landscape-level distribution of groups of blue wildebeest, Connochaetes taurinus, and Burchell's zebra, Equus burchelli, in a predominantly woodland area (Karongwe Game Reserve, South Africa; KGR) to test the hypothesis that group dynamics are a function of minimizing predation risk from their primary predator, lion, Panthera leo.
Methodology/Principal Findings
Using generalized linear models, we examined the relative importance of habitat type (differing in vegetation density), probability of encountering lion (based on utilization distribution of all individual lions in the reserve), and season in predicting group size and composition. We found that only in open scrub habitat, group size for both ungulate species increased with the probability of encountering lion. Group composition differed between the two species and was driven by habitat selection as well as predation risk. For both species, composition of groups was, however, dominated by males in open scrub habitats, irrespective of the probability of encountering lion.
Conclusions/Significance
Distribution patterns of wildebeest and zebra groups at the landscape level directly support the theoretical and empirical evidence from a range of taxa predicting that grouping is favored in open habitats and when predation risk is high. Group composition reflected species-specific social, physiological and foraging constraints, as well as the importance of predation risk. Avoidance of high resource open scrub habitat by females can lead to loss of foraging opportunities, which can be particularly costly in areas such as KGR, where this resource is limited. Thus, landscape-level grouping dynamics are species specific and particular to the composition of the group, arising from a tradeoff between maximizing resource selection and minimizing predation risk.
doi:10.1371/journal.pone.0012758
PMCID: PMC2942830  PMID: 20862216
10.  Increased predation of nutrient-enriched aposematic prey 
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.
doi:10.1098/rspb.2013.3255
PMCID: PMC3953848  PMID: 24598424
educated predator; prey defences; nutrients; toxic prey; mimicry
11.  Are fast explorers slow reactors? Linking personality type and anti-predator behaviour 
Response delays to predator attack may be adaptive, suggesting that latency to respond does not always reflect predator detection time, but can be a decision based on starvation–predation risk trade-offs. In birds, some anti-predator behaviours have been shown to be correlated with personality traits such as activity level and exploration. Here, we tested for a correlation between exploration behaviour and response latency time to a simulated fish predator attack in a fish species, juvenile convict cichlids (Amatitlania nigrofasciata). Individual focal fish were subjected to a standardized attack by a robotic fish predator while foraging, and separately given two repeated trials of exploration of a novel environment. We found a strong positive correlation between exploration and time taken to respond to the predator model. Fish that were fast to explore the novel environment were slower to respond to the predator. Our study therefore provides some of the first experimental evidence for a link between exploration behaviour and predator-escape behaviour. We suggest that different behavioural types may differ in how they partition their attention between foraging and anti-predator vigilance.
doi:10.1098/rspb.2009.1607
PMCID: PMC2842688  PMID: 19864291
personality; shy–bold continuum; anti-predator behaviour; adaptive-response delays; attention; convict cichlid
12.  Intense or Spatially Heterogeneous Predation Can Select against Prey Dispersal 
PLoS ONE  2012;7(1):e28924.
Dispersal theory generally predicts kin competition, inbreeding, and temporal variation in habitat quality should select for dispersal, whereas spatial variation in habitat quality should select against dispersal. The effect of predation on the evolution of dispersal is currently not well-known: because predation can be variable in both space and time, it is not clear whether or when predation will promote dispersal within prey. Moreover, the evolution of prey dispersal affects strongly the encounter rate of predator and prey individuals, which greatly determines the ecological dynamics, and in turn changes the selection pressures for prey dispersal, in an eco-evolutionary feedback loop. When taken all together the effect of predation on prey dispersal is rather difficult to predict. We analyze a spatially explicit, individual-based predator-prey model and its mathematical approximation to investigate the evolution of prey dispersal. Competition and predation depend on local, rather than landscape-scale densities, and the spatial pattern of predation corresponds well to that of predators using restricted home ranges (e.g. central-place foragers). Analyses show the balance between the level of competition and predation pressure an individual is expected to experience determines whether prey should disperse or stay close to their parents and siblings, and more predation selects for less prey dispersal. Predators with smaller home ranges also select for less prey dispersal; more prey dispersal is favoured if predators have large home ranges, are very mobile, and/or are evenly distributed across the landscape.
doi:10.1371/journal.pone.0028924
PMCID: PMC3256147  PMID: 22247764
13.  Mass-dependent predation risk and lethal dolphin–porpoise interactions 
In small birds, mass-dependent predation risk (MDPR) is known to make the trade-off between avoiding starvation and avoiding predation dependent on individual mass. This occurs because carrying increased fat reserves not only reduces starvation risk but also results in a higher predation risk due to reduced escape flight performance and/or the increased foraging exposure needed to maintain a higher body mass. In principle, the theory of MDPR could also apply to any animal capable of storing energy reserves to reduce starvation and whose escape performance decreases with increasing mass. We used a unique situation along certain parts of coastal Britain, where harbour porpoises (Phocoena phocoena) are pursued and killed but crucially not eaten by bottlenose dolphins (Tursiops truncatus), to investigate whether a MDPR effect can occur in non-avian species. We show that where high levels of dolphin ‘predation’ occur, porpoises carry significantly less energy reserves than would otherwise be expected and this equates to reducing by approximately 37% the length of time that a porpoise could survive without feeding. These results provide the first evidence that a mass-dependent starvation–predation risk trade-off may be a general ecological principle that can apply to widely different animal types rather than, as is currently thought, only to birds.
doi:10.1098/rspb.2007.0786
PMCID: PMC2275888  PMID: 17698485
energy reserves; starvation risk; starvation–predation risk trade-off; Phocoena phocoena; Tursiops truncatus
14.  Shrewd alliances: mixed foraging associations between treeshrews, greater racket-tailed drongos and sparrowhawks on Great Nicobar Island, India 
Biology Letters  2009;6(3):304-307.
Mixed-species foraging associations may form to enhance feeding success or to avoid predators. We report the costs and consequences of an unusual foraging association between an endemic foliage gleaning tupaid (Nicobar treeshrew Tupaia nicobarica) and two species of birds; one an insectivorous commensal (greater racket-tailed drongo Dicrurus paradiseus) and the other a diurnal raptor and potential predator (Accipiter sp.). In an alliance driven, and perhaps engineered, by drongos, these species formed cohesive groups with predictable relationships. Treeshrew breeding pairs were found more frequently than solitary individuals with sparrowhawks and were more likely to tolerate sparrowhawks in the presence of drongos. Treeshrews maintained greater distances from sparrowhawks than drongos, and permitted the raptors to come closer when drongos were present. Treeshrew foraging rates declined in the presence of drongos; however, the latter may provide them predator avoidance benefits. The choice of the raptor to join the association is intriguing; particular environmental resource states may drive the evolution of such behavioural strategies. Although foraging benefits seem to be the primary driver of this association, predator avoidance also influences interactions, suggesting that strategies driving the formation of flocks may be complex and context dependent with varying benefits for different actors.
doi:10.1098/rsbl.2009.0945
PMCID: PMC2880059  PMID: 20007167
mixed foraging associations; predator avoidance; context dependence; treeshrews; drongos; sparrowhawks
15.  Social learning in birds and its role in shaping a foraging niche 
We briefly review the literature on social learning in birds, concluding that strong evidence exists mainly for predator recognition, song, mate choice and foraging. The mechanism of local enhancement may be more important than imitation for birds learning to forage, but the former mechanism may be sufficient for faithful transmission depending on the ecological circumstances. To date, most insights have been gained from birds in captivity. We present a study of social learning of foraging in two passerine birds in the wild, where we cross-fostered eggs between nests of blue tits, Cyanistes caeruleus and great tits, Parus major. Early learning causes a shift in the foraging sites used by the tits in the direction of the foster species. The shift in foraging niches was consistent across seasons, as showed by an analysis of prey items, and the effect lasted for life. The fact that young birds learn from their foster parents, and use this experience later when subsequently feeding their own offspring, suggests that foraging behaviour can be culturally transmitted over generations in the wild. It may therefore have both ecological and evolutionary consequences, some of which are discussed.
doi:10.1098/rstb.2010.0343
PMCID: PMC3049099  PMID: 21357219
cultural transmission; ecological niche; foraging conservatism; habitat preferences; speciation
16.  Multiple selective pressures apply to a coral reef fish mimic: a case of Batesian–aggressive mimicry 
Mimics closely resemble unrelated species to avoid predation, capture prey or gain access to hosts or reproductive opportunities. However, the classification of mimicry systems into three established evolutionary mechanisms (protection, reproduction and foraging) can be contentious because multiple benefits may be gained by mimics, causing the evolution of such systems to be driven by more than one selective agent. However, data on such systems are generally speculative or anecdotal. This study provides empirical evidence that dual benefits apply to a coral reef fish mimic in terms of increased access to food (aggressive mimicry) and reduced predation risk (Batesian mimicry). Bicolour fangblennies Plagiotremus laudandus gained access to more reef fish victims, which they attack to feed on fins and scales, when they spent more time associated with their model Meiacanthus atrodorsalis. Furthermore, exact replicas of P. laudandus incurred fewer approaches from potential predators compared with control replicas that varied in resemblance to P. laudandus. Predators with trichromatic visual systems (three distinct spectral sensitivities) could potentially distinguish between replicas based on colour based on theoretical vision models. Therefore, this mimicry system could be best described as Batesian–aggressive mimicry in which mimicry evolution is driven by multiple simultaneous selective pressures.
doi:10.1098/rspb.2009.2218
PMCID: PMC2871877  PMID: 20181564
Batesian mimicry; aggressive mimicry; coral reef fishes; Plagiotremus laudandus; evolution; selective pressures
17.  Daily foraging patterns in free-living birds: exploring the predation–starvation trade-off 
Daily patterns in the foraging behaviour of birds are assumed to balance the counteracting risks of predation and starvation. Predation risks are a function of the influence of weight on flight performance and foraging behaviours that may expose individuals to predators. Although recent research sheds light on daily patterns in weight gain, little data exist on daily foraging routines in free-living birds. In order to test the predictions of various hypotheses about daily patterns of foraging, we quantified the activity of four species of passerines in winter using radio-frequency identification receivers built into supplemental feeding stations. From records of 472 368 feeder visits by tagged birds, we found that birds generally started to feed before sunrise and continued to forage at a steady to increasing rate throughout the day. Foraging in most species terminated well before sunset, suggesting their required level of energy reserves was being reached before the end of the day. These results support the risk-spreading theorem over a long-standing hypothesis predicting bimodality in foraging behaviour purportedly driven by a trade-off between the risks of starvation and predation. Given the increased energetic demands experienced by birds during colder weather, our results suggest that birds' perceptions of risk are biased towards starvation avoidance in winter.
doi:10.1098/rspb.2012.3087
PMCID: PMC3652453  PMID: 23595267
foraging behaviour; starvation–predation trade-off; risk-spreading theorem; resident birds; radio-frequency identification; optimal foraging
18.  The importance of pattern similarity between Müllerian mimics in predator avoidance learning. 
Müllerian mimicry, where unpalatable prey share common warning patterns, has long fascinated evolutionary biologists. It is commonly assumed that Müllerian mimics benefit by sharing the costs of predator education, thus reducing per capita mortality, although there has been no direct test of this assumption. Here, we specifically measure the selection pressure exerted by avian predators on unpalatable prey with different degrees of visual similarity in their warning patterns. Using wild-caught birds foraging on novel patterned prey in the laboratory, we unexpectedly found that pattern similarity did not increase the speed of avoidance learning, and even dissimilar mimics shared the education of naive predators. This was a consistent finding across two different densities of unpalatable prey, although mortalities were lower at the higher density as expected. Interestingly, the mortalities of Müllerian mimics were affected by pattern similarity in the predicted way by the end of our experiment, although the result was not quite significant. This suggests that the benefits to Müllerian mimics may emerge only later in the learning process, and that predator experience of the patterns may affect the degree to which pattern similarity is important. This highlights the need to measure the behaviour of real predators if we are to understand fully the evolution of mimicry systems.
PMCID: PMC1691604  PMID: 15101700
19.  Local adaptation and the potential effects of a contaminant on predator avoidance and antipredator responses under global warming: a space-for-time substitution approach 
Evolutionary Applications  2014;7(3):421-430.
The ability to deal with temperature-induced changes in interactions with contaminants and predators under global warming is one of the outstanding, applied evolutionary questions. For this, it is crucial to understand how contaminants will affect activity levels, predator avoidance and antipredator responses under global warming and to what extent gradual thermal evolution may mitigate these effects. Using a space-for-time substitution approach, we assessed the potential for gradual thermal evolution shaping activity (mobility and foraging), predator avoidance and antipredator responses when Ischnura elegans damselfly larvae were exposed to zinc in a common-garden warming experiment at the mean summer water temperatures of shallow water bodies at southern and northern latitudes (24 and 20°C, respectively). Zinc reduced mobility and foraging, predator avoidance and escape swimming speed. Importantly, high-latitude populations showed stronger zinc-induced reductions in escape swimming speed at both temperatures, and in activity levels at the high temperature. The latter indicates that local thermal adaptation may strongly change the ecological impact of contaminants under global warming. Our study underscores the critical importance of considering local adaptation along natural gradients when integrating biotic interactions in ecological risk assessment, and the potential of gradual thermal evolution mitigating the effects of warming on the vulnerability to contaminants.
doi:10.1111/eva.12141
PMCID: PMC3962302  PMID: 24665344
antipredator traits; ecological risk assessment; escape speed; global warming; latitudinal gradient; metals; predator avoidance; space-for-time substitution; thermal adaptation
20.  Evolving the selfish herd: emergence of distinct aggregating strategies in an individual-based model 
From zebra to starlings, herring and even tadpoles, many creatures move in an organized group. The emergent behaviour arises from simple underlying movement rules, but the evolutionary pressure which favours these rules has not been conclusively identified. Various explanations exist for the advantage to the individual of group formation: reduction of predation risk; increased foraging efficiency or reproductive success. Here, we adopt an individual-based model for group formation and subject it to simulated predation and foraging; the haploid individuals evolve via a genetic algorithm based on their relative success under such pressure. Our work suggests that flock or herd formation is likely to be driven by predator avoidance. Individual fitness in the model is strongly dependent on the presence of other phenotypes, such that two distinct types of evolved group can be produced by the same predation or foraging conditions, each stable against individual mutation. We draw analogies with multiple Nash equilibria theory of iterated games to explain and categorize these behaviours. Our model is sufficient to capture the complex behaviour of dynamic collective groups, yet is flexible enough to manifest evolutionary behaviour.
doi:10.1098/rspb.2007.0306
PMCID: PMC2169279  PMID: 17472913
flocking; evolution; genetic algorithm; predation; foraging; Nash equilibrium
21.  Plant Defenses and Predation Risk Differentially Shape Patterns of Consumption, Growth, and Digestive Efficiency in a Guild of Leaf-Chewing Insects 
PLoS ONE  2014;9(4):e93714.
Herbivores are squeezed between the two omnipresent threats of variable food quality and natural enemy attack, but these two factors are not independent of one another. The mechanisms by which organisms navigate the dual challenges of foraging while avoiding predation are poorly understood. We tested the effects of plant defense and predation risk on herbivory in an assemblage of leaf-chewing insects on Solanum lycopersicum (tomato) that included two Solanaceae specialists (Manduca sexta and Leptinotarsa decemlineata) and one generalist (Trichoplusia ni). Defenses were altered using genetic manipulations of the jasmonate phytohormonal cascade, whereas predation risk was assessed by exposing herbivores to cues from the predaceous stink bug, Podisus maculiventris. Predation risk reduced herbivore food intake by an average of 29% relative to predator-free controls. Interestingly, this predator-mediated impact on foraging behavior largely attenuated when quantified in terms of individual growth rate. Only one of the three species experienced lower body weight under predation risk and the magnitude of this effect was small (17% reduction) compared with effects on foraging behavior. Manduca sexta larvae, compensated for their predator-induced reduction in food intake by more effectively converting leaf tissue to body mass. They also had higher whole-body lipid content when exposed to predators, suggesting that individuals convert energy to storage forms to draw upon when risk subsides. In accordance with expectations based on insect diet breadth, plant defenses tended to have a stronger impact on consumption and growth in the generalist than the two specialists. These data both confirm the ecological significance of predators in the foraging behavior of herbivorous prey and demonstrate how sophisticated compensatory mechanisms allow foragers to partially offset the detrimental effects of reduced food intake. The fact that these mechanisms operated across a wide range of plant resistance phenotypes suggests that compensation is not always constrained by reduced food quality.
doi:10.1371/journal.pone.0093714
PMCID: PMC3981721  PMID: 24718036
22.  The three-dimensional flight of red-footed boobies: adaptations to foraging in a tropical environment? 
In seabirds a broad variety of morphologies, flight styles and feeding methods exist as an adaptation to optimal foraging in contrasted marine environments for a wide variety of prey types. Because of the low productivity of tropical waters it is expected that specific flight and foraging techniques have been selected there, but very few data are available. By using five different types of high-precision miniaturized logger (global positioning systems, accelerometers, time depth recorders, activity recorders, altimeters) we studied the way a seabird is foraging over tropical waters. Red-footed boobies are foraging in the day, never foraging at night, probably as a result of predation risks. They make extensive use of wind conditions, flying preferentially with crosswinds at median speed of 38 km h−1, reaching highest speeds with tail winds. They spent 66% of the foraging trip in flight, using a flap–glide flight, and gliding 68% of the flight. Travelling at low costs was regularly interrupted by extremely active foraging periods where birds are very frequently touching water for landing, plunge diving or surface diving (30 landings h−1). Dives were shallow (maximum 2.4 m) but frequent (4.5 dives h−1), most being plunge dives. While chasing for very mobile prey like flying fishes, boobies have adopted a very active and specific hunting behaviour, but the use of wind allows them to reduce travelling cost by their extensive use of gliding. During the foraging and travelling phases birds climb regularly to altitudes of 20–50 m to spot prey or congeners. During the final phase of the flight, they climb to high altitudes, up to 500 m, probably to avoid attacks by frigatebirds along the coasts. This study demonstrates the use by boobies of a series of very specific flight and activity patterns that have probably been selected as adaptations to the conditions of tropical waters.
doi:10.1098/rspb.2004.2918
PMCID: PMC1634943  PMID: 15875570
tracking; global positioning system; accelerometers; altitude; wind; prey capture
23.  Hitting the buffers: conspecific aggression undermines benefits of colonial breeding under adverse conditions 
Biology Letters  2008;4(6):630-633.
Colonial breeding in birds is widely considered to benefit individuals through enhanced protection against predators or transfer of information about foraging sites. This view, however, is largely based on studies of seabirds carried out under favourable conditions. Recent breeding failures at many seabird colonies in the UK provide an opportunity to re-examine costs and benefits of coloniality under adverse conditions. Common guillemots Uria aalge are highly colonial cliff-nesting seabirds with very flexible parental care. Although the single chick is normally never left alone, more than 50 per cent of offspring were left unattended at a North Sea colony in 2007, apparently because poor conditions forced both parents to forage simultaneously. Contrary to expectation, unattended chicks were not killed by avian predators. Rather, although non-breeders and failed breeders sometimes provided alloparental care, unattended chicks were frequently attacked by breeding guillemots at neighbouring sites, often with fatal consequences. These results highlight a previously unsuspected trade-off between provisioning chicks and avoiding conspecific attacks, and indicate that understanding how environmental conditions affect social dynamics is crucial to interpreting costs and benefits of colonial breeding.
doi:10.1098/rsbl.2008.0417
PMCID: PMC2614172  PMID: 18796390
density dependence; social dynamics; chick neglect; infanticide; environmental change
24.  Ecological and hormonal correlates of antipredator behavior in adult Belding’s ground squirrels (Spermophilus beldingi) 
Predator–prey relationships provide an excellent opportunity to study coevolved adaptations. Decades of theoretical and empirical research have illuminated the various behavioral adaptations exhibited by prey animals to avoid detection and capture, and recent work has begun to characterize physiological adaptations, such as immune reactions, metabolic changes, and hormonal responses to predators or their cues. A 2-year study quantified the activity budgets and antipredator responses of adult Belding’s ground squirrels (Spermophilus beldingi) living in three different California habitats and likely experiencing different predation pressures. At one of these sites, which is visually closed and predators and escape burrows are difficult to see, animals responding to alarm calls remain alert longer and show more exaggerated responses than adults living in two populations that likely experience less intense predation pressure. They also spend more time alert and less time foraging than adults at the other two sites. A 4-year study using noninvasive fecal sampling of cortisol metabolites revealed that S. beldingi living in the closed site also have lower corticoid levels than adults at the other two sites. The lower corticoids likely reflect that predation risk at this closed site is predictable, and might allow animals to mount large acute cortisol responses, facilitating escape from predators and enhanced vigilance while also promoting glucose storage for the approaching hibernation. Collectively, these data demonstrate that local environments and perceived predation risk influence not only foraging, vigilance, and antipredator behaviors, but adrenal functioning as well, which may be especially important for obligate hibernators that face competing demands on glucose storage and mobilization.
doi:10.1007/s00265-007-0436-9
PMCID: PMC2844651  PMID: 20336174
Spermophilus; Fecal cortisol; Antipredator strategies; Population differences
25.  Effects of Selection for Honey Bee Worker Reproduction on Foraging Traits 
PLoS Biology  2008;6(3):e56.
The “reproductive ground plan” hypothesis (RGPH) proposes that reproductive division of labour in social insects had its antecedents in the ancient gene regulatory networks that evolved to regulate the foraging and reproductive phases of their solitary ancestors. Thus, queens express traits that are characteristic of the reproductive phase of solitary insects, whereas workers express traits characteristic of the foraging phase. The RGPH has also been extended to help understand the regulation of age polyethism within the worker caste and more recently to explain differences in the foraging specialisations of individual honey bee workers. Foragers that specialise in collecting proteinaceous pollen are hypothesised to have higher reproductive potential than individuals that preferentially forage for nectar because genes that were ancestrally associated with the reproductive phase are active. We investigated the links between honey bee worker foraging behaviour and reproductive traits by comparing the foraging preferences of a line of workers that has been selected for high rates of worker reproduction with the preferences of wild-type bees. We show that while selection for reproductive behaviour in workers has not altered foraging preferences, the age at onset of foraging of our selected line has been increased. Our findings therefore support the hypothesis that age polyethism is related to the reproductive ground plan, but they cast doubt on recent suggestions that foraging preferences and reproductive traits are pleiotropically linked.
Author Summary
In social insects, the evolution of the worker caste and the regulation of reproductive behaviour by workers are poorly understood. Evolution is conservative and often proceeds by adapting an existing gene network to a new function. The “reproductive ground plan” hypothesis (RGPH) suggests that social insects evolved their queen and worker castes by modifying a gene network that once regulated the foraging and reproductive phases of solitary ancestors. In this model, queens retain characteristics of insects in their reproductive phase, whereas workers retain characteristics of the foraging phase. Moreover, the foraging behaviour of workers may also be regulated by the same genes that once controlled the switch between foraging and feeding young in the nest. We evaluated the RGPH by studying a line of honey bees selected for high rates of worker reproduction. We show that in this line workers forage late in life and some may never forage, supporting the idea that genes related to reproduction are also related to foraging. However, we found no support for recent suggestions that genes related to reproduction also regulate the foraging behaviour of individual workers: once they start foraging, our highly reproductive workers forage in the same way that unselected workers do.
A new study lends support to the model of social insect evolution, in which a gene regulatory network linked to the reproductive and foraging phases of ancestral solitary insects gave rise to queen and worker castes. But the study challenges the notion that genes related to reproduction also regulate the foraging behavior of workers.
doi:10.1371/journal.pbio.0060056
PMCID: PMC2270312  PMID: 18318602

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