Multimodal Floral Signals and Moth Foraging Decisions

Background

Combinations of floral traits – which operate as attractive signals to pollinators – act on multiple sensory modalities. For Manduca sexta hawkmoths, how learning modifies foraging decisions in response to those traits remains untested, and the contribution of visual and olfactory floral displays on behavior remains unclear.

Methodology/Principal Findings

Using M. sexta and the floral traits of two important nectar resources in southwestern USA, Datura wrightii and Agave palmeri, we examined the relative importance of olfactory and visual signals. Natural visual and olfactory cues from D. wrightii and A. palmeri flowers permits testing the cues at their native intensities and composition – a contrast to many studies that have used artificial stimuli (essential oils, single odorants) that are less ecologically relevant. Results from a series of two-choice assays where the olfactory and visual floral displays were manipulated showed that naïve hawkmoths preferred flowers displaying both olfactory and visual cues. Furthermore, experiments using A. palmeri flowers – a species that is not very attractive to hawkmoths – showed that the visual and olfactory displays did not have synergistic effects. The combination of olfactory and visual display of D. wrightii, however – a flower that is highly attractive to naïve hawkmoths – did influence the time moths spent feeding from the flowers. The importance of the olfactory and visual signals were further demonstrated in learning experiments in which experienced moths, when exposed to uncoupled floral displays, ultimately chose flowers based on the previously experienced olfactory, and not visual, signals. These moths, however, had significantly longer decision times than moths exposed to coupled floral displays.

Conclusions/Significance

These results highlight the importance of specific sensory modalities for foraging hawkmoths while also suggesting that they learn the floral displays as combinatorial signals and use the integrated floral traits from their memory traces to mediate future foraging decisions.     

Segregating the Effects of Seed Traits and Common Ancestry of Hardwood Trees on Eastern Gray Squirrel Foraging Decisions

The evolution of specific seed traits in scatter-hoarded tree species often has been attributed to granivore foraging behavior. However, the degree to which foraging investments and seed traits correlate with phylogenetic relationships among trees remains unexplored. We presented seeds of 23 different hardwood tree species (families Betulaceae, Fagaceae, Juglandaceae) to eastern gray squirrels (Sciurus carolinensis), and measured the time and distance travelled by squirrels that consumed or cached each seed. We estimated 11 physical and chemical seed traits for each species, and the phylogenetic relationships between the 23 hardwood trees. Variance partitioning revealed that considerable variation in foraging investment was attributable to seed traits alone (27–73%), and combined effects of seed traits and phylogeny of hardwood trees (5–55%). A phylogenetic PCA (pPCA) on seed traits and tree phylogeny resulted in 2 “global” axes of traits that were phylogenetically autocorrelated at the family and genus level and a third “local” axis in which traits were not phylogenetically autocorrelated. Collectively, these axes explained 30–76% of the variation in squirrel foraging investments. The first global pPCA axis, which produced large scores for seed species with thin shells, low lipid and high carbohydrate content, was negatively related to time to consume and cache seeds and travel distance to cache. The second global pPCA axis, which produced large scores for seeds with high protein, low tannin and low dormancy levels, was an important predictor of consumption time only. The local pPCA axis primarily reflected kernel mass. Although it explained only 12% of the variation in trait space and was not autocorrelated among phylogenetic clades, the local axis was related to all four squirrel foraging investments. Squirrel foraging behaviors are influenced by a combination of phylogenetically conserved and more evolutionarily labile seed traits that is consistent with a weak or more diffuse coevolutionary relationship between rodents and hardwood trees rather than a direct coevolutionary relationship.     

Use of Social and Ecological Information in Tamarin Foraging Decisions

A major consequence of group living is that foragers may rely on social information in addition to ecological information to locate feeding sites. Although conspecifics can provide cues as to the spatial location of food patches, individual foraging decisions also must include some assessment of the likelihood of obtaining access to a resource other group members seek. This likelihood differs in the 2 models generally proposed to explain intragroup social foraging: the information-sharing model and the producer-scrounger model. We conducted an experimental field study on wild groups of emperor (Saguinus imperator) and saddleback (S. fuscicollis) tamarins to determine the foraging strategies adopted by individual group members and their relationship to social rank, food intake, and the ability to use ecological and social information in making intra-patch foraging decisions. Individual tamarins applied different behavioral strategies compatible with a finder-joiner paradigm to solve foraging problems. About half of the individuals in each study group initiated 74%–90% of all food searches and acted as finders. Most alpha individuals adopted a joiner strategy by monitoring the activities of others' to obtain a reward. The individual arriving first at a reward platform enjoyed a finder's advantage. Despite differences in search effort, both finders and joiners presented similar abilities in learning to associate ecological cues with the presence of food rewards at our experimental feeding stations. We conclude that within a group foraging context, tamarins integrate social and ecological information in decision-making.     

When Parasitoid Males Make Decisions: Information Used when Foraging for Females

Optimal foraging models predict how an organism allocates its time and energy while foraging for aggregated resources. These models have been successfully applied to organisms such as predators looking for prey, female parasitoids looking for hosts, or herbivorous searching for food. In this study, information use and patch time allocation were investigated using male parasitoids looking for mates. The influence of the former presence of females in absence of mates and the occurrence of mating and other reproductive behaviours on the patch leaving tendency was investigated for the larval parasitoid Asobara tabida. Although males do not modify their patch residence time based on the number of females that visited the patch, they do show an increase in the patch residence time after mating a virgin female and performing courtship behaviour such as opening their wings. These results are in concordance with an incremental mechanism, as it has been described for females of the same species while foraging for hosts. The similarities between males and females of the same species, and the conditions under which such a patch-leaving decision rule is fitted are discussed. This is the first study describing an incremental effect of mating on patch residence time in males, thus suggesting that similar information use are probably driving different organisms foraging for resource, regardless of its nature.     

Spillover Effects of Loss of Control on Risky Decision-Making

Decision making in risky situations is frequently required in our everyday lives and has been shown to be influenced by various factors, some of which are independent of the risk context. Based on previous findings and theories about the central role of perceptions of control and their impact on subsequent settings, spillover effects of subjective loss of control on risky decision-making are assumed. After developing an innovative experimental paradigm for inducing loss of control, its hypothesized effects on risky decision-making are investigated. Partially supporting the hypotheses, results demonstrated no increased levels of risk perceptions but decreased risk-taking behavior following experiences of loss of control. Thus, this study makes a methodological contribution by proposing a newly developed experimental paradigm facilitating further research on the effects of subjective loss of control, and additionally provides partial evidence for the spillover effects of loss of control experiences on risky decision-making.     

Memory Effects on Movement Behavior in Animal Foraging

An individual’s choices are shaped by its experience, a fundamental property of behavior important to understanding complex processes. Learning and memory are observed across many taxa and can drive behaviors, including foraging behavior. To explore the conditions under which memory provides an advantage, we present a continuous-space, continuous-time model of animal movement that incorporates learning and memory. Using simulation models, we evaluate the benefit memory provides across several types of landscapes with variable-quality resources and compare the memory model within a nested hierarchy of simpler models (behavioral switching and random walk). We find that memory almost always leads to improved foraging success, but that this effect is most marked in landscapes containing sparse, contiguous patches of high-value resources that regenerate relatively fast and are located in an otherwise devoid landscape. In these cases, there is a large payoff for finding a resource patch, due to size, value, or locational difficulty. While memory-informed search is difficult to differentiate from other factors using solely movement data, our results suggest that disproportionate spatial use of higher value areas, higher consumption rates, and consumption variability all point to memory influencing the movement direction of animals in certain ecosystems.     

Risky Decisions and Their Consequences: Neural Processing by Boys with Antisocial Substance Disorder

Background

Adolescents with conduct and substance problems (“Antisocial Substance Disorder” (ASD)) repeatedly engage in risky antisocial and drug-using behaviors. We hypothesized that, during processing of risky decisions and resulting rewards and punishments, brain activation would differ between abstinent ASD boys and comparison boys.

Methodology/Principal Findings

We compared 20 abstinent adolescent male patients in treatment for ASD with 20 community controls, examining rapid event-related blood-oxygen-level-dependent (BOLD) responses during functional magnetic resonance imaging. In 90 decision trials participants chose to make either a cautious response that earned one cent, or a risky response that would either gain 5 cents or lose 10 cents; odds of losing increased as the game progressed. We also examined those times when subjects experienced wins, or separately losses, from their risky choices. We contrasted decision trials against very similar comparison trials requiring no decisions, using whole-brain BOLD-response analyses of group differences, corrected for multiple comparisons. During decision-making ASD boys showed hypoactivation in numerous brain regions robustly activated by controls, including orbitofrontal and dorsolateral prefrontal cortices, anterior cingulate, basal ganglia, insula, amygdala, hippocampus, and cerebellum. While experiencing wins, ASD boys had significantly less activity than controls in anterior cingulate, temporal regions, and cerebellum, with more activity nowhere. During losses ASD boys had significantly more activity than controls in orbitofrontal cortex, dorsolateral prefrontal cortex, brain stem, and cerebellum, with less activity nowhere.

Conclusions/Significance

Adolescent boys with ASD had extensive neural hypoactivity during risky decision-making, coupled with decreased activity during reward and increased activity during loss. These neural patterns may underlie the dangerous, excessive, sustained risk-taking of such boys. The findings suggest that the dysphoria, reward insensitivity, and suppressed neural activity observed among older addicted persons also characterize youths early in the development of substance use disorders.     

Bottleneck Effects on Genetic Variance for Courtship Repertoire

Bottleneck effects on evolutionary potential in mating behavior were addressed through assays of additive genetic variances and resulting phenotypic responses to drift in the courtship repertoires of six two-pair founder-flush lines and two control populations of the housefly. A simulation addressed the complication that an estimate of the genetic variance for a courtship trait (e.g., male performance vigor or the female requirement for copulation) must involve assays against the background behavior of the mating partners. The additive ``environmental' effect of the mating partner's phenotype simply dilutes the net parent-offspring covariance for a trait. However, if there is an interaction with this ``environmental' component, negative parent-offspring covariances can result under conditions of high incompatibility between the population's distributions for male performance and female choice requirements, despite high levels of genetic variance. All six bottlenecked lines exhibited significant differentiation from the controls in at least one measure of the parent-offspring covariance for male performance or female choice (estimated by 50 parent-son and 50 parent-daughter covariances for 10 courtship traits per line) which translated to significant phenotypic drift. However, the average effect across traits or across lines did not yield a significant net increase in genetic variance due to bottlenecks. Concerted phenotypic differentiation due to the founder-flush event provided indirect evidence of directional dominance in a subset of traits. Furthermore, indirect evidence of genotype-environment interactions (potentially producing genotype-genotype effects) was found in the negative parent-offspring covariances predicted by the male-female interaction simulation and by the association of the magnitude of phenotypic drift with the absolute value of the parent-offspring covariance. Hence, nonadditive genetic effects on mating behavior may be important in structuring genetic variance for courtship, although most of the increases in genetic variance would be expected to reflect inbreeding depression with relatively rare situations representing the facilitation of speciation by bottlenecks.     

The Impact of Physiological Demands on Foraging Decisions under Predation Risk: A Test with the Whelk Acanthina monodon

We study whether and how physiological demands affect foraging decisions under predation risk, by evaluating the effect of starvation on the rate of food consumption and prey‐size preferences and the potential trade‐off between starvation and predation risk on foraging behavior in the whelk Acanthina monodon, a gastropod inhabiting the intertidal rocky shores of central Chile. These whelks appear to adjust their foraging strategy to physiological (nutritional) demand and predation risk. Starvation reduced the effect of predation risk on the rate of food consumption by A. monodon. Thus, in the absence of the predator sea star, the rate of food consumption by starved and satiated whelks was similar. When a predator was present, starved whelks fed faster than satiated whelks. Our results indicate that foraging behaviour represents an integrated and hierarchical response to environmental conditions and the physiological conditions of the forager.     

Using Past Experience in Web Relocation Decisions Enhances the Foraging Efficiency of the Spider Cyclosa argenteoalba

The purpose of this study is to test whether the integration of past and present foraging experience in web relocation decision enhances foraging efficiency of the spider Cyclosa argenteoalba in its natural environment. We measured daily changes in the prey availability at several fixed sites in a natural environment and constructed a model environment based on these observational data. In the model environment, we simulated the behavior of spiders that foraged and relocated their webs according to several decision rules, which differed in terms of how a spider used its past experience. Results of the simulation revealed that the less past experience is discounted in making web relocation decisions, the more prey the spider is expected to capture. The expected number of web relocations decreased as spiders kept past foraging experience longer. These results suggest that C. argenteoalba enhances foraging efficiency by using past foraging experience for long times in the decision of web relocation in its natural environment.     

Paternal Genetic Effects on Foraging Decision-Making Under the Risk of Predation

Foraging behavior under the risk of predation has interested biologists for decades. Here, we examine paternal genetic effects on foraging decisions of bluegill (Lepomis macrochirus) larvae sired by males adopting alternative life histories. We use split in vitro fertilization to generate maternal half‐siblings sired by either a ‘parental’ male or a ‘cuckolder’ male. Immediately, upon the switch to exogenous feeding, we fed the larvae ad libitum for 2 d. We then starved the larvae for between 12 and 17 h, following which we subjected them to a dichotomous choice foraging trial, where one side of a test tank posed a risky foraging habitat and the other posed a safe foraging habitat. Equal amounts of food were simultaneously introduced to both sides of the tank and the proportion of individuals on either side was recorded. There were significantly fewer cuckolder offspring foraging on the risky side of the tank when compared with their parental half‐siblings indicating that cuckolder offspring took fewer risks than parental offspring. These results demonstrate a paternal genetic effect (sire life history) on foraging behavior. We ruled out energetic state as a possible explanation for this difference because the half‐siblings did not differ in body length or mass. Instead, previous research suggests that cuckolder offspring have higher conversion efficiency (efficiency of converting food into soma) than parental offspring and therefore the differences in foraging behavior observed here may, in part, be attributed to genetic differences in conversion efficiency.     

性状遗传力与QTL方差对标记辅助选择效果的影响

在采用动物模型标记辅助最佳线性无偏预测方法对个体育种值进行估计的基础上,模拟了在一个闭锁群体内连续对单个性状选择10个世代的情形,并系统地比较了性状遗传力和QTL方差对标记辅助选择所获得的遗传进展、QTL增效基因频率和群体近交系数变化的影响。结果表明：在对高遗传力和QTL方差较小的性状实施标记辅助选择时,可望获得更大的遗传进展;遗传力越高,QTL方差越大,则QTL增效基因频率的上升速度越快;遗传力较高时,群体近交系数上升的速度较为缓慢,而QTL方差对群体近交系数上升速度的影响则不甚明显。结合前人关于标记辅助选择相对效率的研究结果,可以认为：当选择性状的遗传力和QTL方差为中等水平时,标记辅助选择可望获得理想的效果。     

Potential Foraging Decisions by a Desert Ungulate to Balance Water and Nutrient Intake in a Water-Stressed Environment

Arid climates have unpredictable precipitation patterns, and wildlife managers often provide supplemental water to help desert ungulates endure the hottest, driest periods. When surface water is unavailable, the only source of water for ungulates comes from the forage they consume, and they must make resourceful foraging decisions to meet their requirements. We compared two desert bighorn sheep (Ovis canadensis nelsoni) populations in Arizona, USA: a treatment population with supplemental water removed during treatment, and a control population. We examined whether sheep altered their seasonal diets without supplemental water. We calculated water and nutrient intake and metabolic water production from dry matter intake and forage moisture and nitrogen content, to determine whether sheep could meet their seasonal daily water and nutrient requirements solely from forage. Diets of sheep were higher in protein (all seasons) and moisture (autumn and winter) during treatment compared to pretreatment. During treatment, sheep diet composition was similar between the treatment and control populations, which suggests, under the climatic conditions of this study, water removal did not influence sheep diets. We estimated that under drought conditions, without any surface water available (although small ephemeral potholes would contain water after rains), female and male sheep would be unable to meet their daily water requirements in all seasons, except winter, when reproductive females had a nitrogen deficit. We determined that sheep could achieve water and nutrient balances in all seasons by shifting their total diet proportions by 8–55% from lower to higher moisture and nitrogen forage species. We elucidate how seasonal forage quality and foraging decisions by desert ungulates allow them to cope with their xeric and uncertain environment, and suggest that, with the forage conditions observed in our study area during this study period, providing supplemental water during water-stressed periods may not be necessary for desert bighorn sheep.     

Effects of Mixed-species Foraging Groups on the Feeding and Aggression of Juvenile Parrotfishes

Many parrotfishes (Scaridae) co-occur in mixed-species aggregations as juveniles, but diverge in resource use and social structure as adults. Focal observations of three juvenile parrotfishes (Scarus coeruleus, Sparisoma aurofrenatum, and Sparisoma viride) were conducted on inshore patch reefs in the Florida Keys to determine how feeding and aggressive interactions vary with group participation. All three species spent more time in groups than alone, most often in groups of less than ten individuals. Feeding rates were significantly higher for S. viride when foraging in groups than when alone. All species fed most often from Halimeda, and overall diet composition was similar for fish whether feeding in groups or alone. The frequency of aggressive interactions varied with group participation. Focal S. aurofrenatum were more aggressive when in groups than when alone, and both S. aurofrenatum and S. viride were attacked more often by damselfishes when they were alone than when in groups. In contrast, feeding rates, diet breadth, and aggressive interactions of S. coeruleus were less affected by group participation. Small mixed-species aggregations of coral reef fishes may be large enough for individuals to assume some of the benefits of group participation while at the same time avoiding the costs of competition realized in larger groups.     

Determination of Foraging Thresholds and Effects of Application on Energetic Carrying Capacity for Waterfowl

Energetic carrying capacity of habitats for wildlife is a fundamental concept used to better understand population ecology and prioritize conservation efforts. However, carrying capacity can be difficult to estimate accurately and simplified models often depend on many assumptions and few estimated parameters. We demonstrate the complex nature of parameterizing energetic carrying capacity models and use an experimental approach to describe a necessary parameter, a foraging threshold (i.e., density of food at which animals no longer can efficiently forage and acquire energy), for a guild of migratory birds. We created foraging patches with different fixed prey densities and monitored the numerical and behavioral responses of waterfowl (Anatidae) and depletion of foods during winter. Dabbling ducks (Anatini) fed extensively in plots and all initial densities of supplemented seed were rapidly reduced to 10 kg/ha and other natural seeds and tubers combined to 170 kg/ha, despite different starting densities. However, ducks did not abandon or stop foraging in wetlands when seed reduction ceased approximately two weeks into the winter-long experiment nor did they consistently distribute according to ideal-free predictions during this period. Dabbling duck use of experimental plots was not related to initial seed density, and residual seed and tuber densities varied among plant taxa and wetlands but not plots. Herein, we reached several conclusions: 1) foraging effort and numerical responses of dabbling ducks in winter were likely influenced by factors other than total food densities (e.g., predation risk, opportunity costs, forager condition), 2) foraging thresholds may vary among foraging locations, and 3) the numerical response of dabbling ducks may be an inconsistent predictor of habitat quality relative to seed and tuber density. We describe implications on habitat conservation objectives of using different foraging thresholds in energetic carrying capacity models and suggest scientists reevaluate assumptions of these models used to guide habitat conservation.     

Effects of Environmental Complexity and Temporary Captivity on Foraging Behavior of Wild-Caught Meadow Voles

Increased housing of wild nonhuman animals in captivity for conservation, research, and rehabilitation has revealed the importance of systematically analyzing effects of the captive environment on behavior. This study focused on the effects of complexity and time held in captivity on foraging behaviors of wild-caught, adult meadow voles (Microtus pennsylvanicus). Forty-six individuals captured from a meadow outside Oshkosh, WI, were assigned to 1 of 4 captive treatment groups: simple/<50 days (SS), simple/>50 days, complex/<50 days, and complex/>50 days. Number of dish visits, proportion foraging, and frequency of nonforaging behaviors recorded during a 15-min foraging trial were measured for all subjects. Kruskal-Wallis and Mann-Whitney U Tests were conducted to analyze 4 different comparisons within this behavioral data. Overall, neither time in captivity or environmental complexity affected nonforaging behaviors. In contrast, foraging behaviors did change with treatment: Voles were less active at food dishes and visited control dishes more in treatment group SS than in the other treatment groups. In addition, sex-related differences in foraging behaviors were maintained when voles were exposed to environmental complexity. This article includes options for wildlife managers to adapt captive environments to meet the welfare and behavioral needs of translocated wild nonhuman mammals.     

Non-Consumptive Predator Effects Shape Honey Bee Foraging and Recruitment Dancing

Predators can reduce bee pollination and plant fitness through successful predation and non-consumptive effects. In honey bees, evidence of predation or a direct attack can decrease recruitment dancing and thereby magnify the effects of individual predation attempts at a colony level. However, actual predation attempts and successes are relatively rare. It was not known if a far more common event, just detection of a predator, could inhibit recruitment. We began by testing honey bees'' avoidance of the praying mantis (Tenodera sinensis). Larger predators (later mantis instars, ≥4.5 cm in body length) elicited significantly more avoidance (1.3 fold) than smaller mantis instars. Larger instars also attempted to capture honey bees significantly more often than did smaller instars. Foragers could detect and avoid mantises based upon mantis odor (74% of bees avoided an odor extract) or visual appearance (67% avoided a mantis model). Finally, foragers decreased recruitment dancing by 1.8 fold for a food source with a live adult mantis, even when they were not attacked. This reduction in recruitment dancing, elicited by predator presence alone, expands our understanding of predator non-consumptive effects and of cascading ecosystem effects for plants served by an important generalist pollinator.