Cues of Predation Risk Induce Instar‐ and Genotype‐Specific Changes in Pea Aphid Colony Spatial Structure

Deploying collective antipredator behaviors during periods of increased predation risk is a major determinant of individual fitness for most animal groups. Pea aphids, Acyrthosiphon pisum, which live in aggregations of genetically identical individuals produced via asexual reproduction warn nearby conspecifics of pending attack by secreting a volatile alarm pheromone. This alarm pheromone allows clone‐mates to evade predation by walking away or dropping off the host plant. Here, we test how a single alarm pheromone emission influences colony structure and defensive behavior in this species. Relative to control colonies, groups exposed to alarm pheromone exhibited pronounced escape behavior where many individuals relocated to adjacent leaves on the host plant. Alarm pheromone reception, however, also had subtle instar‐specific effects: The proportion of 1st instars feeding nearest the leaf petiole decreased as these individuals moved to adjacent leaves, while the proportion of 2nd–3rd instars feeding nearest the leaf petiole remained constant. Fourth instars also dispersed to neighboring leaves after pheromone exposure. Lastly, alarm pheromone reception caused maternal aphids to alter their preferred feeding sites in a genotype‐specific manner: Maternal aphids of the green genotype fed further from the petiole, while maternal aphids of the pink genotype fed closer to the petiole. Together, our results suggest that aphid colony responses to alarm pheromone constitute a diversity of nuanced instar‐ and genotype‐specific effects. These behavioral responses can dramatically change the spatial organization of colonies and their collective defensive behavior.     

Fitness costs and benefits of shelter building and leaf trenching behaviour in a pyralid caterpillar

1. Shelter building and petiole trenching in the Lepidoptera is a behaviour that mediates ecological pressures including those exerted by both food plants and natural enemies. 2. Fitness costs and benefits of trenching and shelter‐building behaviour related to predation and larval performance were investigated in a pyralid species that inhabits and feeds on leaf shelters. 3. Assays comparing the performance of caterpillars feeding on trenched versus non‐trenched foliage and fresh versus dry leaves were conducted. Whereas pupal weight was positively affected by petiole trenching, larval development was delayed when caterpillars fed on dry leaves. 4. A field experiment comparing predation on caterpillars inside and outside shelters demonstrated that predation was significantly higher for exposed caterpillars. 5. No physiological costs associated with shelter building were found given that caterpillars performed equally regardless of the number of shelters they built. 6. The effect sizes of top‐down and bottom‐up forces on pupal weight, development time, and predation risk indicated that the major effect of shelters is through the reduction of predation risk. The integration of experiments and natural history observations showed that fitness benefits provided by shelters change across ontogeny.     

Transgenerational Behavioral Plasticity in a Parthenogenetic Insect in Response to Increased Predation Risk

Reliable cues of increased predation risk can induce phenotypic changes in an organism’s offspring (i.e. transgenerational phenotypic plasticity). While induction of defensive morphologies in naïve offspring in response to maternal predation risk is widespread, little is known about transgenerational changes in offspring behavior. Here we provide evidence for transgenerational behavioral plasticity in the pea aphid, Acyrthosiphon pisum. When pre-reproductive individuals of two genotypes (“pink” and “green”) were exposed to the alarm pheromone (E)-β-Farnesene (EBF), a reliable cue of increased predation risk, next-generation offspring altered their feeding site choices relative to the location of the maternal aphids. Offspring of EBF-treated aphids occupied “safer” feeding sites: green offspring occupied “safer” feeding sites in the natal colony, while pink offspring dispersed to occupy sites on neighboring plant leaves.     

Cool Headed Individuals Are Better Survivors: Non-Consumptive and Consumptive Effects of a Generalist Predator on a Sap Feeding Insect

Non-consumptive effects (NCEs) of predators are part of the complex interactions among insect natural enemies and prey. NCEs have been shown to significantly affect prey foraging and feeding. Leafhopper''s (Auchenorrhyncha) lengthy phloem feeding bouts may play a role in pathogen transmission in vector species and also exposes them to predation risk. However, NCEs on leafhoppers have been scarcely studied, and we lack basic information about how anti-predator behaviour influences foraging and feeding in these species. Here we report a study on non-consumptive and consumptive predator-prey interactions in a naturally co-occurring spider–leafhopper system. In mesocosm arenas we studied movement patterns during foraging and feeding of the leafhopper Psammotettix alienus in the presence of the spider predator Tibellus oblongus. Leafhoppers delayed feeding and fed much less often when the spider was present. Foraging movement pattern changed under predation risk: movements became more frequent and brief. There was considerable individual variation in foraging movement activity. Those individuals that increased movement activity in the presence of predators exposed themselves to higher predation risk. However, surviving individuals exhibited a ‘cool headed’ reaction to spider presence by moving less than leafhoppers in control trials. No leafhoppers were preyed upon while feeding. We consider delayed feeding as a “paradoxical” antipredator tactic, since it is not necessarily an optimal strategy against a sit-and-wait generalist predator.     

Foraging Patch Selection in Winter: A Balance between Predation Risk and Thermoregulation Benefit

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.     

Predation Risk Perception,Food Density and Conspecific Cues Shape Foraging Decisions in a Tropical Lizard

When foraging, animals can maximize their fitness if they are able to tailor their foraging decisions to current environmental conditions. When making foraging decisions, individuals need to assess the benefits of foraging while accounting for the potential risks of being captured by a predator. However, whether and how different factors interact to shape these decisions is not yet well understood, especially in individual foragers. Here we present a standardized set of manipulative field experiments in the form of foraging assays in the tropical lizard Anolis cristatellus in Puerto Rico. We presented male lizards with foraging opportunities to test how the presence of conspecifics, predation-risk perception, the abundance of food, and interactions among these factors determines the outcome of foraging decisions. In Experiment 1, anoles foraged faster when food was scarce and other conspecifics were present near the feeding tray, while they took longer to feed when food was abundant and when no conspecifics were present. These results suggest that foraging decisions in anoles are the result of a complex process in which individuals assess predation risk by using information from conspecific individuals while taking into account food abundance. In Experiment 2, a simulated increase in predation risk (i.e., distance to the feeding tray) confirmed the relevance of risk perception by showing that the use of available perches is strongly correlated with the latency to feed. We found Puerto Rican crested anoles integrate instantaneous ecological information about food abundance, conspecific activity and predation risk, and adjust their foraging behavior accordingly.     

Antipredator responses of aphids to parasitoids change as a function of aphid physiological state

Under predation risk, prey may prioritize antipredator behaviours and sacrifice feeding. However, energetically constrained animals may choose to sacrifice or change antipredator responses and accept relatively greater risk in order to secure food. In this last case, the antipredator tactics chosen must balance safety and feeding in such a way that costs are minimized and benefits maximized. We studied the antipredator behaviour of pea aphid, Acyrthosiphon pisum (Harris) (Hemiptera: Aphididae) subjected to different periods of food deprivation, against the parasitoid Aphidius ervi (Hymenoptera: Braconidae). As the energetic internal stress of aphids increased, the predominant antipredator response changed from walking away and dropping to kicking behaviour, and parasitization avoidance decreased. Parasitoids did not show preference between food-deprived and nonfood-deprived aphids. Dropping and walking away reduced parasitization from 50 to 33%. These results support the hypothesis that the antipredator behaviour of an aphid changes as a function of internal stress. By performing less costly behaviour such as kicking under energetically constrained conditions, aphids seem to minimize their probability of energy shortfall. Given that aphid antipredator behaviour is a function of nutritional state, its occurrence under natural conditions may match host quality spatial distribution. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Aphid responses to volatile cues from turnip plants (Brassica rapa) infested with phloem-feeding and chewing herbivores

Herbivore-induced plant volatiles provide foraging cues for herbivores and for herbivores’ natural enemies. Aphids induce plant volatile emissions and also utilize plant-derived olfactory volatile cues, but the chemical ecology of aphids and other phloem-feeding insects is less extensively documented than that of chewing insects. Here, we characterize the volatile cues emitted by turnip plants (Brassica rapa) under attack by an aphid (Myzus persicae) or by the chewing lepidopteran larva Heliothis virescens. We also tested the behavioral responses of M. persicae individuals to the odors of undamaged and herbivore-damaged plants presented singly or in combination, as well as to the odor of crushed conspecifics (simulating predation). Gas chromatographic analysis of the volatile blend of infested turnips revealed distinct profiles for both aphid- and caterpillar-induced plants, with induced compounds including green-leaf alcohols, esters, and isothiocyanates. In behavioral trials, aphids exhibited increased activity in the presence of plant odors and positive attraction to undamaged turnip plants. However, aphids exhibited a strong preference for the odors of healthy versus plants subjected to herbivore damage, and neither aphid- or caterpillar-damaged plants were attractive compared to clean-air controls. Reduced aphid attraction to herbivore-infested plants may be mediated by changes in the volatile blend constituent composition, including large amounts of isothiocyanates and green-leaf volatiles or, in the case of aphid-infested plants, of the aphid alarm pheromone, (E)-β-farnesene.     

Population expansion in the North African Late Pleistocene signalled by mitochondrial DNA haplogroup U6

Background

Altruistic anti-predatory behaviours pose an evolutionary problem because they are costly to the actor and beneficial to the recipients. Altruistic behaviours can evolve through indirect fitness benefits when directed toward kin. The altruistic nature of anti-predatory behaviours is often difficult to establish because the actor can obtain direct fitness benefits, or the behaviour could result from selfish coercion by others, especially in eusocial animals. Non-eusocial parthenogenetically reproducing aphids form colonies of clone-mates, which are ideal to test the altruistic nature of anti-predatory defence behaviours. Many aphids release cornicle secretions when attacked by natural enemies such as parasitoids. These secretions contain an alarm pheromone that alerts neighbours (clone-mates) of danger, thereby providing indirect fitness benefits to the actor. However, contact with cornicle secretions also hampers an attacker and could provide direct fitness to the actor.

Results

We tested the hypothesis that cornicle secretions are altruistic by assessing direct and indirect fitness consequences of smearing cornicle secretions onto an attacker, and by manipulating the number of clone-mates that could benefit from the behaviour. We observed parasitoids, Aphidius rhopalosiphi, foraging singly in patches of the cereal aphid Sitobion avenae of varied patch size (2, 6, and 12 aphids). Aphids that smeared parasitoids did not benefit from a reduced probability of parasitism, or increase the parasitoids' handling time. Smeared parasitoids, however, spent proportionately more time grooming and less time foraging, which resulted in a decreased host-encounter and oviposition rate within the host patch. In addition, individual smearing rate increased with the number of clone-mates in the colony.

Conclusions

Cornicle secretions of aphids were altruistic against parasitoids, as they provided no direct fitness benefits to secretion-releasing individuals, only indirect fitness benefits through neighbouring clone-mates. Moreover, the use of cornicle secretions was consistent with their altruistic nature, because the occurrence of this behaviour increased with the size of indirect fitness benefits, the number of clone-mates that can benefit. This study provides evidence for a case of kin-directed altruistic defence outside eusocial animals.     

Linking recruitment to trophic factors: revisiting the Beverton--Holt recruitment model from a life history and multispecies perspective

The Beverton--Holt recruitment model can be derived from arguments about evolution of life history traits related to foraging and predation risk, along with spatially localized and temporarily competitive relationships in the habitats where juvenile fish forage and face predation risk while foraging. This derivation explicitly represents two key biotic factors, food supply (I) and predator abundance (R), which appear as a risk ratio (R/I) that facilitates modelling of changes in trophic circumstances and analysis of historical data. The same general recruitment relationship is expected whether the juvenile life history is simple or involves a complex sequence of stanzas; in the complex case, the Beverton--Holt parameters represent weighted averages or integrals of risk ratios over the stanzas. The relationship should also apply in settings where there is complex, mesoscale variation in habitat and predation risk, provided that animals sense this variation and move about so as to achieve similar survival at all mesoscale rearing sites. The model predicts that changes in food and predation risk can be amplified violently in settings where juvenile survival rate is low, producing large changes in recruitment rates over time.     

Pea aphid dropping behavior diminishes foraging efficiency of a predatory ladybeetle

Antipredator defensive behaviors are a well‐studied and often crucial part of prey life histories, but little has been done to quantify how such behaviors affect natural enemies, their foraging, and their effectiveness as biological control agents. We explored how the generalist predatory coccinellid Harmonia axyridis Pallas (Coleoptera: Coccinellidae) affects the dropping behavior of the pea aphid, Acyrthosiphon pisum (Harris) (Homoptera: Aphididae), and in turn, how that defensive behavior affects the foraging efficiency of the predator. Experimental arenas that allowed or prevented pea aphid dropping were compared to determine how dropping influences the foraging of multiple life stages of H. axyridis: second instars, fourth instars, and adults. Dropping reduced predation on aphids by all ladybeetle life stages. Despite older predators inducing more dropping, aphid dropping reduced predation by approximately 40% across all ladybeetle life stages. Aphid dropping and predator consumption of aphids were both correlated with how much the predator moved, which also increased with predator life stage. We suggest that the high rates of dropping induced by H. axyridis and the subsequent decrease in H. axyridis foraging efficiency may partially explain why H. axyridis is less effective at controlling pea aphids than it is at controlling other aphid species that do not drop.     

Factors influencing leaf vein selection in the lime aphid (Eucallipterus tiliae L.)

Summary The thickness of sclerenchyma around the veins of lime leaves varies with both size of leaf and size of vein and may provide a barrier to stylet penetration. Although small veins confer greater nutritional benefits and have no lignified barriers, there are advantages to feeding on the larger veins for those more mature aphids which can penetrate the sclerenchyma. Feeding on the large veins of the upper surface, which are situated in grooves, may provide protection against dislodgement. On the undersurfaces of small leaves, feeding on large veins promotes orientation towards the petiole and early warning of approaching predators. On the corresponding surfaces of large leaves the sclerenchyma is thicker but aphids can achieve orientation by feeding on the smallest veins.     

The Influence of Previous Experience and Starvation on Aphid Feeding Behavior

It was hypothesized that (1) previous experience of aphids on a host plant leads to differences in their feeding behavior relative to aphids without previous experience on it and that (2) a change in the physiological state of the aphid modifies their experience-induced behavior. Using electronic recording, the feeding behavior of the aphid Sitobion fragariae (Walker) on wheat Triticum aestivum L. and oat Avena sativa L. was examined, comparing aphids with or without previous experience on a given host and with or without a period of starvation before assessing probing behavior. All comparisons were performed within a single aphid clone to minimize the effect of genetic variation. Feeding behavior on wheat was significantly affected by previous experience and starvation. The effect of previous experience interacted with the host plant where feeding behavior was tested. Aphids feeding on wheat following previous experience on wheat showed a longer time and a higher number of pathway activities and less time in waveform F (i.e., mechanical stylet work and penetration difficulties) than did aphids feeding on wheat after a previous experience on oat. No differences in the time from the beginning of the recording until the first salivation into the sieve elements were found. When aphids were subjected to a period of starvation, the time devoted to xylem ingestion increased compared with that of nonconstrained aphids. These results are discussed in terms of factors affecting foraging decisions.     

Prey size affects the costs and benefits of group predation in nymphs of the predatory stink bug Andrallus spinidens (Heteroptera: Pentatomidae)

Group predation promotes foraging efficiency because it increases the size of prey that can be killed and improves hunting success compared to solitary predation. However, group predation may increase competition among group members during feeding. Earlier studies have focused on the advantages of group predation, but little is known about the costs and benefits of group predation for individual members of the group. Here, we show that the costs and benefits of group predation for individuals of the predatory stink bug Andrallus spinidens vary with prey size in laboratory experiments. We found that when A. spinidens fed on small prey, group predation did not significantly increase foraging efficiency but did increase competition for food among group members. In contrast, when prey was large, group predation promoted foraging efficiency, and competition over food was not detected. Our results suggest that group predation by A. spinidens nymphs is advantageous for individual members because it enables each member to hunt larger prey that could not be hunted alone. However, when group size was large or prey size was small, group predation increased competition among group members.     

Worth the reward? An experimental assessment of risk‐taking behavior along a life history gradient

Life history theory predicts that species with faster life history strategies should be willing to risk their survival more to acquire resources than those with slower life history strategies. Foraging can be a risky behavior and animals generally face a tradeoff between food consumption and predation risk. We predicted that the degree to which animals invest in current versus future reproduction (i.e. life history strategy) would determine how they approach this tradeoff. We manipulated food abundance in wetlands to assess whether life history theory could explain risk taking among females of five duck species with respect to foraging. We found evidence consistent with our prediction based on life history theory; species with a faster life history strategy were willing to engage in riskier behavior, by feeding more intensively, for a greater food reward. Females from species with faster life history strategies devoted 25% more time to feeding when in high food density treatment plots versus control plots. The percentage of time that females from species with slower life history strategies devoted to feeding was not affected by food density. These findings contribute to our understanding of life history theory and represent a possible mechanism to explain differences in life history strategies among species.     

小麦蚜虫田间调查及监测技术

小麦蚜虫是世界范围内小麦生产中一类重要害虫。针对麦蚜世代历期短、繁殖力强,具有趋光、趋化及迁飞等生物学及行为习性;在田间多呈聚集分布,且麦蚜易受寄主植物抗性、天敌、气象因素及农田生态条件等生物与非生物因素影响等发生为害特点,本文阐述了我国小麦蚜虫田间调查、监测技术及防治策略,以期为我国小麦蚜虫综合防控提供基础科学支撑。     

Cornicle length in Macrosiphini aphids: a comparison of ecological traits

Abstract 1. Aphids often emit cornicle droplets when attacked by predators. While the function of cornicle droplets has long been debated (i.e. mechanical protection vs. chemical signalling), it is not understood why aphid species have cornicles of different lengths.
2. It was hypothesised that aphids living in more scattered colonies have longer cornicles to scent-mark predators with cornicle droplets containing alarm pheromone, so that clone-mates are provided with advanced warning of a threat, even if not at the predation site. To test this hypothesis, multiple regression analyses were used, due to a lack of phylogenetic information on these taxa, to address which ecological traits (amount of wax on an aphid, degree of colony aggregation, feeding shelter, ant attendance) are correlated with cornicle length.
3. Aphids living in dense colonies tended to have shorter cornicles than aphids living in more scattered colonies. Also, aphids with more protection (i.e. wax) on their bodies had shorter cornicles. Aphids also tended to have shorter cornicles when tended by ants. The presence of a feeding shelter was not a good predictor of cornicle length.
4. It is suggested that longer cornicles function to scent-mark predators with alarm pheromone to increase the inclusive fitness of a clone; however the negative correlation between the amount of individual protection, and also ant attendance, and cornicle length argues for a trade-off between different forms of defence.     

Season- and size-dependent risk taking in juvenile coho salmon: experimental evaluation of asset protection

Using juvenile coho salmon, Oncorhynchus kisutch, we tested predictions arising from dynamic optimization models of foraging under predation risk. Coho juveniles from two size groups raised in the laboratory were individually fed varying food rations. Their willingness to risk predation was measured as the time to resume foraging after presentation of a predator model. Small fish (mean weight 1.5 g) resumed feeding earlier than larger fish (3.5 g) as predicted by dynamic models under summer photoperiod but not under autumn photoperiod. Contrary to predictions, larger fish did not increase risk taking and small fish decreased risk taking between summer and autumn treatments. Food ration significantly influenced time to resume feeding only in small coho. A simple mechanistic model we proposed to explain feeding motivation under risk as a function of body size and prior growth rate was not sufficient to explain observed variation in risk taking. This study suggests that coho salmon use photoperiod and their own body size as cues for long-term, state-dependent adjustments of feeding behaviour. The lower risk taking of larger fish is probably an example of asset protection, whereby larger animals accept less predation risk to protect their greater accumulated fitness value. The decrease of risk taking in small fish in the autumn was possibly caused by a switch of life history trajectory towards delayed smolting. Copyright 1999 The Association for the Study of Animal Behaviour.     

Predator-induced morphological shift in the pea aphid

Aphids exhibit a polymorphism whereby individual aphids are either winged or unwinged. The winged dispersal morph is mainly responsible for the colonization of new plants and, in many species, is produced in response to adverse environmental conditions. Aphids are attacked by a wide range of specialized predators and predation has been shown to strongly influence the growth and persistence of aphid colonies. In two experiments, we reared two clones of pea aphid (Acyrthosiphon pisum) in the presence and absence of predatory ladybirds (Coccinella septempunctata or Adalia bipunctata). In both experiments, the presence of a predator enhanced the proportion of winged morphs among the offspring produced by the aphids. The aphid clones differed in their reaction to the presence of a ladybird, suggesting the presence of genetic variation for this trait. A treatment that simulated disturbance caused by predators did not enhance winged offspring production. The experiments indicate that aphids respond to the presence of a predator by producing the dispersal morph which can escape by flight to colonize other plants. In contrast to previous examples of predator-induced defence this shift in prey morphology does not lead to better protection against predator attack, but enables aphids to leave plants when mortality risks are high.     

Plant Defenses and Predation Risk Differentially Shape Patterns of Consumption,Growth, and Digestive Efficiency in a Guild of Leaf-Chewing Insects

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.