Look before you leap: is risk of injury a foraging cost?

Theory states that an optimal forager should exploit a patch so long as its harvest rate of resources from the patch exceeds its energetic, predation, and missed opportunity costs for foraging. However, for many foragers, predation is not the only source of danger they face while foraging. Foragers also face the risk of injuring themselves. To test whether risk of injury gives rise to a foraging cost, we offered red foxes pairs of depletable resource patches in which they experienced diminishing returns. The resource patches were identical in all respects, save for the risk of injury. In response, the foxes exploited the safe patches more intensively. They foraged for a longer time and also removed more food (i.e., had lower giving up densities) in the safe patches compared to the risky patches. Although they never sustained injury, video footage revealed that the foxes used greater care while foraging from the risky patches and removed food at a slower rate. Furthermore, an increase in their hunger state led foxes to allocate more time to foraging from the risky patches, thereby exposing themselves to higher risks. Our results suggest that foxes treat risk of injury as a foraging cost and use time allocation and daring—the willingness to risk injury—as tools for managing their risk of injury while foraging. This is the first study, to our knowledge, which explicitly tests and shows that risk of injury is indeed a foraging cost. While nearly all foragers may face an injury cost of foraging, we suggest that this cost will be largest and most important for predators.     

Ideal free distributions under predation risk

 We examine the trade-off between gathering food and avoiding predation in the context of patch use by a group of animals. Often a forager will have to choose between feeding sites that differ in both energetic gain rate and predation risk. The ideal site will have a high gain rate and low risk of predation. However, intake rate will often decrease when the patch is shared with other foragers and it may be optimal for some individuals to feed elsewhere. Within the framework of ideal free theory, we investigate the distribution of foragers that will equalise individual fitness gains. We focus on a two-patch environment with continuous inputs of food. With reference to existing experimental studies, we examine the effects of risk dilution, food input rates and an animal’s expectations of the future. We identify the effect of total animal numbers when one patch is subject to predation risk and the other is safe. Conditions under which the difference in intake rate in the two patches is constant are identified, as are conditions in which the ratio of animals in the two patches is constant. If current conditions do not alter future expectations an increase in input rates to the patches promotes increased use of the risky patch. Yet, if conditions are assumed to persist indefinitely the opposite effect is seen. When both patches are subject to predation risk, dilution of risk favours more extreme distributions, and may lead to more than one stable distribution. The results of these models are used to critically analyse previous work on the energetic equivalence of risk. This paper is intended to help guide the development of new experimental studies into the energy-risk trade-off. Received: 10 February 1995/Accepted after revision: 1 October 1995     

Division of foraging labor in ants can mediate demands for food and safety

Solitary foragers can balance demands for food and safety by varying their relative use of foraging patches and their level of vigilance. Here, we investigate whether colonies of the ant, Formica perpilosa, can balance these demands by dividing labor among workers. We show that foragers collecting nectar in vegetation near their nest are smaller than are those collecting nectar at sites away from the nest. We then use performance tests to show that smaller workers are more likely to succumb to attack from conspecifics but feed on nectar more efficiently than larger workers, suggesting a size-related trade-off between risk susceptibility and harvesting ability. Because foragers that travel away from the nest are probably more likely to encounter ants from neighboring colonies, this trade-off could explain the benefits of dividing foraging labor among workers. In a laboratory experiment, we show that contact with aggressive workers results in an increase in the mean size of recruits to a foraging site: this increase was not the result of more large recruits, but rather because fewer smaller ants traveled to the site. These results suggest that workers particularly susceptible to risk avoid dangerous sites, and suggest that variation in worker size can allow colonies to exploit profitably both hazardous and resource-poor patches.Communicated by L. Sundström     

Patch choice under perceptual constraints: a cause for departures from an ideal free distribution

Summary A review of tests of ideal free distribution (IFD) theory reveals a characteristic bias: patches with a small proportion of the resources are relatively overused and patches with a larger proportion of the resources are relatively underused. A model is developed to examine how animals with limited abilities to perceive differences in patch quality affect an IFD by foragers. This constraint produces the observed bias, a bias that is exaggerated as the number of patches increases. Sutherland (1983) has developed a model based on interference which can also explain the observed bias. The two models can be differentiated in that only the perception limit model (this paper) is sensitive to absolute changes in overall resource availability and to increases in the number of animals. Additionally, Sutherland's model predicts that when deviations away from an IFD occur there will be no differences in intake rates, while the perception limit model predicts that intake rates should vary between patches.     

Foraging tactics of two guilds of web-spinning spiders

Summary The foraging behavior of orbweaving and sheetweb weaving guilds of spiders was investigated. Orbweavers move among web-sites frequently, but sheetweb weavers do not. A simple model that examines the adaptive advantages of active foraging and sit-and-wait strategies leads to three predictions: 1) Orbweavers should have a simple decision rule for leaving web-sites, 2) Orbweavers' web-sites should have more variable payoffs than do the web-sites of sheetweb weavers, and 3) Orbweavers should have a lower cost of moving than do sheetweb weavers. Field and experimental data bear out each prediction. In addition, analysis of the residence times of spiders at web-sites that are used more than once reveals that members of the two guilds do not compete with each other for web-sites.The distinction between active foragers and sit-and-wait predators stems from the relative frequency of the decision to leave a foraging site. Thus active foragers are those predators that move often from patch to patch, and sit-and-wait predators are those that leave patches infrequently. In this sense, orbweaving spiders are active foragers and sheetweb weavers are sit-and-wait predators.     

Optimal movement strategies for social foragers in unpredictable environments

Spatial movement models often base movement decision rules on traditional optimal foraging theories, including ideal free distribution (IFD) theory, more recently generalized as density-dependent habitat selection (DDHS) theory, and the marginal value theorem (MVT). Thus optimal patch departure times are predicted on the basis of the density-dependent resource level in the patch. Recently, alternatives to density as a habitat selection criterion, such as individual knowledge of the resource distribution, conspecific attraction, and site fidelity, have been recognized as important influences on movement behavior in environments with an uncertain resource distribution. For foraging processes incorporating these influences, it is not clear whether simple optimal foraging theories provide a reasonable approximation to animal behavior or whether they may be misleading. This study compares patch departure strategies predicted by DDHS theory and the MVT with evolutionarily optimal patch departure strategies for a wide range of foraging scenarios. The level of accuracy with which individuals can navigate toward local food sources is varied, and individual tendency for conspecific attraction or repulsion is optimized over a continuous spectrum. We find that DDHS theory and the MVT accurately predict the evolutionarily optimal patch departure strategy for foragers with high navigational accuracy for a wide range of resource distributions. As navigational accuracy is reduced, the patch departure strategy cannot be accurately predicted by these theories for environments with a heterogeneous resource distribution. In these situations, social forces improve foraging success and have a strong influence on optimal patch departure strategies, causing individuals to stay longer in patches than the optimal foraging theories predict.     

Manuscript in preparation for <Emphasis Type="Italic">Behavioral Ecology and Sociobiology</Emphasis> Bumble bee pollen foraging regulation: role of pollen quality,storage levels,and odor

The regulation of protein collection through pollen foraging plays an important role in pollination and in the life of bee colonies that adjust their foraging to natural variation in pollen protein quality and temporal availability. Bumble bees occupy a wide range of habitats from the Nearctic to the Tropics in which they play an important role as pollinators. However, little is known about how a bumble bee colony regulates pollen collection. We manipulated protein quality and colony pollen stores in lab-reared colonies of the native North American bumble bee, Bombus impatiens. We debut evidence that bumble bee colony foraging levels and pollen storage behavior are tuned to the protein quality (range tested: 17–30% protein by dry mass) of pollen collected by foragers and to the amount of stored pollen inside the colony. Pollen foraging levels (number of bees exiting the nest) significantly increased by 55%, and the frequency with which foragers stored pollen in pots significantly increased by 233% for pollen with higher compared to lower protein quality. The number of foragers exiting the nest significantly decreased (by 28%) when we added one pollen load equivalent each 5 min to already high intranidal pollen stores. In addition, pollen odor pumped into the nest is sufficient to increase the number of exiting foragers by 27%. Foragers directly inspected pollen pots at a constant rate over 24 h, presumably to assess pollen levels. Thus, pollen stores can act as an information center regulating colony-level foraging according to pollen protein quality and colony need. An erratum to this article can be found at     

Integrated modelling of foraging behaviour, energy budget and memory properties

A predator's foraging performance is related to its ability to acquire sufficient information on environmental profitability. This process can be affected by the patchy distribution and clustering of food resources and by the food intake process dynamics.We simulated body mass growth and behaviour in a forager acting in a patchy environment with patchy distribution of both prey abundance and body mass by an individual-based model. In our model, food intake was a discrete and stochastic process and leaving decision was based on the estimate of net energy gain and searching time during their foraging activities. The study aimed to investigate the effects of learning processes and food resource exploitation on body mass and survival of foragers under different scenarios of intra-patch resource distribution.The simulation output showed that different sources of resource variability between patches affected foraging efficiency differently. When prey abundance varied across patches, the predator stayed longer in poorest patches to obtain the information needed and its performance was affected by the cost of sampling and the resulting assessment of the environment proved unreliable. On the other hand, when prey body mass, but not abundance, varied among the patches the predator was quickly able to assess local profitability. Both body mass and survival of the predator were greatly affected by learning processes and patterns of food resource distribution.     

Persistent bimodal activity patterns in wild and captive black-tailed godwit <Emphasis Type="Italic">Limosa limosa</Emphasis> under different environmental conditions

There is a large literature dealing with daily foraging routines of wild birds during the non-breeding season. While different laboratory studies have showed that some bird activity patterns are a persistent property of the circadian system, most of field studies preclude the potential role of an endogenous circadian rhythm in controlling bird’s foraging routines. In this study we compared the patterns of diurnal foraging activity and intake rates of migrating black-tailed godwits, Limosa limosa (radio-tagged and non-tagged individuals) at two stopover sites (habitats) with different environmental characteristics, aiming at identifying proximate factors of bird activity routines. To gain insights into the role of food availability in control of such foraging routines, we also estimated foraging activity patterns in captive godwits subjected to constant food availability. Captive and wild black-tailed godwits showed a persistent bimodal activity pattern through daylight period. Food availability had a significant effect on the intake rates, but had a subtler effect on foraging and intake rate rhythms. Temperature and wind speed (combined in a weather index) showed non-significant effects on both rhythms. Although we could not discard a role for natural diurnal changes in light intensity, an important timing cue, our findings support the idea that an endogenous circadian rhythm could be an important proximate factor regulating foraging activity and food items taken per unit time of wild black-tailed godwits during migration.     

The influence of pollen quality on foraging behavior in honeybees (Apis mellifera L.)

Individual and colony-level foraging behaviors were evaluated in response to changes in the quantity or nutritional quality of pollen stored within honeybee (Apis mellifera L.) colonies. Colonies were housed in vertical, three-frame observation hives situated inside a building, with entrances leading to the exterior. Before receiving treatments, all colonies were deprived of pollen for 5 days and pollen foragers were marked. In one treatment group, colony pollen reserves were quantitatively manipulated to a low or high level, either by starving colonies of pollen or by providing them with a fully provisioned frame of pollen composed of mixed species. In another treatment group, pollen reserves were qualitatively manipulated by removing pollen stores from colonies and replacing them with low- or high-protein pollen supplements. After applying treatments, foraging rates were measured four times per day and pollen pellets were collected from experienced and inexperienced foragers to determine their weight, species composition, and protein content. Honeybee colonies responded to decreases in the quantity or quality of pollen reserves by increasing the proportion of pollen foragers in their foraging populations, without increasing the overall foraging rate. Manipulation of pollen stores had no effect on the breadth of floral species collected by colonies, or their preferences for the size or protein content of pollen grains. In addition, treatments had no effect on the weight of pollen loads collected by individual foragers or the number of floral species collected per foraging trip. However, significant changes in foraging behavior were detected in relation to the experience level of foragers. Irrespective of treatment group, inexperienced foragers exerted greater effort by collecting heavier pollen loads and also sampled their floral environment more extensively than experienced foragers. Overall, our results indicate that honeybees respond to deficiencies in the quantity or quality of their pollen reserves by increasing the gross amount of pollen returned to the colony, rather than by specializing in collecting pollen with a greater protein content. Individual pollen foragers appear to be insensitive to the quality of pollen they collect, indicating that colony-level feedback is necessary to regulate the flow of protein to and within the colony. Colonies may respond to changes in the quality of their pollen stores by adjusting the numbers of inexperienced to experienced foragers within their foraging populations.     

Social foraging by honeybees: how colonies allocate foragers among patches of flowers

Summary To understand how a colony of honeybees keeps its forager force focussed on rich sources of food, and analysis was made of how the individual foragers within a colony decide to abandon or continue working (and perhaps even recruit to) patches of flowers. A nectar forager grades her behavior toward a patch in response to both the nectar intake rate of her colony and the quality of her patch. This results in the threshold in patch quality for acceptance of a patch being higher when the colonial intake rate of nectar is high than when it is low. Thus colonies can adjust their patch selectivity so that they focus on rich sources when forage is abundant, but spread their workers among a wider range of sources when forage is scarce. Foragers assess their colony's rate of nectar intake while in the nest, unloading nectar to receiver bees. The ease of unloading varies inversely with the colonial intake rate of nectar. Foragers assess patch quality while in the field, collecting nectar. By grading their behavior steeply in relation to such patch variables as distance from the nest and nectar sweetness, foragers give their colony high sensitivity to differences in profitability among patches. When a patch's quality declines, its foragers reduce their rate of visits to the patch. This diminishes the flow of nectar from the poor patch which in turn stimulates recruitment to rich patches. Thus a colony can swiftly redistribute its forager force following changes in the spatial distribution of rich food sources. The fundamental currency of nectar patch quality is not net rate of energy intake, (Gain-Cost)/Time, but may be net energy efficiency, (Gain-Cost)/Cost.     

Avian flocking reduces starvation risk: an experimental demonstration

Summary Theory suggests that variance in individual food intake is lower during group foraging. Consequently, group foraging can at times reduce starvation risk. In aviary experiments using green-finches we demonstrate how intake variability decreases during group foraging because individuals use feeding by flock mates as a cue to locate food (local enhancement). Flocking preferences of greenfinches responded to variance in energy gain as predicted by theoretical models for foragers attempting to reduce starvation risk. While energy budget was positive the greenfinches were risk averse and foraged socially. Their preference shifted towards more risk prone solitary foraging when kept on a negative energy budget. We conclude that time or energy net gains are not necessary for foraging groups to form, but reductions in starvation risk may be sufficient.     

Optimal patch time allocation for time-limited foragers

The Charnov Marginal Value Theorem (MVT) predicts the optimal foraging duration of animals exploiting patches of resources. The predictions of this model have been verified for various animal species. However, the model is based on several assumptions that are likely too simplistic. One of these assumptions is that animals are living forever (i.e., infinite horizon). Using a simple dynamic programming model, we tested the importance of this assumption by analysing the optimal strategy for time-limited foragers. We found that, for time-limited foragers, optimal patch residence times should be greater than those predicted from the classic, static MVT, and the deviation should increase when foragers are approaching the end of their life. These predictions were verified for females of the parasitoid Anaphes victus (Hymenoptera: Mymaridae) exploiting egg patches of its host, the carrot weevil Listronotus oregonensis (Coleoptera: Curculionidae). As predicted by the model, females indeed remained for a longer time on host patches when they approached the end of their life. Experimental results were finally analysed with a Cox regression model to identify the patch-leaving decision rules females used to behave according to the model’s predictions.     

Foraging in the seed-harvester ant genus Pogonomyrmex: are energy costs important?

Energy intake and expenditure on natural foraging trips were estimated for the seed-harvester ants, Pogonomyrmex maricopa and P. rugosus. During seed collection, P. maricopa foraged individually, whereas P. rugosus employed a trunk-trail foraging system. Energy gain per trip and per minute were not significantly different between species. There was also no interspecific difference in energy cost per trip, but energy cost per minute was lower for P. maricopa foragers because they spent on average 7 min longer searching for a load on each trip. Including both unsuccessful and successful foraging trips, average energy gain per trip was more than 100 times the energy cost per trip for both species. Based on this result, we suggest that time cost incurred during individual foraging trips is much more important than energy cost in terms of maximizing net resource intake over time. In addition, because energy costs are so small relative to gains, we propose that energy costs associated with foraging may be safely ignored in future tests of foraging theory with seed-harvesting ant species.     

Past experiences and future expectations generate context-dependent costs of foraging

Because environments can vary over space and time in non-predictable ways, foragers must rely on estimates of resource availability and distribution to make decisions. Optimal foraging theory assumes that foraging behavior has evolved to maximize fitness and provides a conceptual framework in which environmental quality is often assumed to be fixed. Another more mechanistic conceptual framework comes from the successive contrast effects (SCE) approach in which the conditions that an individual has experienced in the recent past alter its response to current conditions. By regarding foragers’ estimation of resource patches as subjective future value assessments, SCE may be integrated into an optimal foraging framework to generate novel predictions. We released Allenby’s gerbils (Gerbillus andersoni allenbyi) into an enclosure containing rich patches with equal amounts of food and manipulated the quality of the environment over time by reducing the amount of food in most (but not all) food patches and then increasing it again. We found that, as predicted by optimal foraging models, gerbils increased their foraging activity in the rich patch when the environment became poor. However, when the environment became rich again, the gerbils significantly altered their behavior compared to the first identical rich period. Specifically, in the second rich period, the gerbils spent more time foraging and harvested more food from the patches. Thus, seemingly identical environments can be treated as strikingly different by foragers as a function of their past experiences and future expectations.     

Dominance and the dynamics of phenotype-limited distribution in common cranes

We studied the behavior of 13 radiotagged cranes dispersing from a communal roost over days when they changed their main daily foraging area between consecutive days during two winter seasons. Individuals went to a new foraging zone when on the previous day their morning food intake had fallen below their mean morning food intake measured over the whole winter. Food intake on the day before a change in foraging area was positively correlated with dominance rank. Dominant cranes changed to new zones with higher numbers of birds and food density, while subordinate cranes went to new zones with lower numbers of birds. As a result, all birds increased their food intake over that of the previous day. Dominant cranes remained more faithful to their most preferred foraging zone, where they spent 69% of the mornings, while subordinate birds were more mobile, switching among zones frequently. Dominant birds left the roost later than subordinate birds on the days they changed to a new zone, which could be used to track the main departing flows. The results suggest that the dynamics that led to a truncated phenotype-limited distribution were determined by social dominance and food abundance, with dominant cranes shifting to a new zone to maintain their high intake levels and subordinates changing more frequently whenever their daily intake did not reach the minimum metabolic requirements. Received: 16 December 1996 / Accepted after revision: 22 February 1997     

A field investigation of scrounging in semipalmated sandpipers

Animals that forage in groups can produce their own food patches or scrounge the food discoveries of their companions. Mean tactic payoffs are expected to be the same at equilibrium for phenotypically equal foragers. Scrounging is also typically viewed as a risk-averse foraging strategy that provides a more even food intake rate over time. The occurrence of scrounging and the payoffs from different foraging modes have rarely been investigated in the field. Over two field seasons, I examined patch sharing in semipalmated sandpipers (Calidris pusilla) foraging on minute food items at the surface of the substrate. Birds could find patches on their own, a producing event, or join the food patches discovered by others, a scrounging event. I found that the average search time per patch did not differ between producing and scrounging but that the average time spent exploiting a patch was reduced nearly by half when scrounging. As a result, the proportion of time spent exploiting a patch, a measure of foraging payoffs, was significantly lower when scrounging. The variance in payoffs was similar for producing and scrounging. When producing their own patches, individuals that scrounged spent the same proportion of time exploiting a patch as those that only produced. However, within the same individuals, the search time for a scrounged patch was longer than the search time for a produced patch. The results show unequal payoffs for producing and scrounging in this system and suggest that low success in finding patches elicited scrounging.     

Nonlinear effects of food aggregation on interference competition in mallards

Previous studies of interference competition have shown an asymmetric effect on intake rate of foragers on clumped resources, with only subordinate individuals suffering. However, the food distributions in these studies were uniform or highly clumped, whereas in many field situations, food aggregation is intermediate. Here we investigated whether food distribution (i.e., uniform, slightly clumped, and highly clumped) affects the behavioral response of mallards foraging alone or competing with another. Although the amount of food was the same in all distributions, the mallards reached higher intake rates, visited fewer patches, and showed longer average feeding times in the highly clumped distribution. Competing mallards had lower intake rates on the slightly clumped than on the uniform or highly clumped food distributions. Subordinates generally visited more patches and had shorter feeding times per patch, but their intake rates were not significantly lower than those of dominants. Therefore, we propose that subordinates do not necessarily suffer from interference competition in terms of intake rate, but do suffer higher search costs. In addition, although dominants had significantly higher average feeding times on the best quality patches of the highly clumped food distribution, such an effect was not found in the slightly clumped distribution. These findings indicate that in environments where food is aggregated to a lesser extent, monopolization is not the best strategy for dominants. Our results suggest that interference experiments should use food distributions that resemble the natural situation animals are faced with in the field.     

Migratory fuelling in blackcaps (Sylvia atricapilla) under perceived risk of predation

It has been argued that the body mass levels achieved by birds are determined by the trade-off between risks of starvation and predation. Birds have also been found to reduce body mass in response to an increased predation risk. During migration, the need of extra fuel for flights is obvious and crucial. In this study, migratory blackcaps (Sylvia atricapilla) were subject to an experimental stopover situation where the predation risk was manipulated by exposure to a stuffed predator. Blackcaps that perceived an imminent risk of predation increased their food intake and fuel deposition rate during the first period of stopover compared with a control group. The pattern of night activity indicates that birds that were exposed to the predator also chose to leave earlier than birds in the control group. Since there was no cover present at the stopover site, birds might have perceived the risk of predation as higher regardless of whether they were foraging or not. Under such circumstances it has been predicted that birds should increase their foraging activity. The findings in this study clearly indicate that birds are able to adjust their stopover behaviour to perceived predation risk. Received: 8 January 1997 / Accepted after revision: 11 April 1997     

Colony nutritional status modulates worker responses to foraging recruitment pheromone in the bumblebee Bombus terrestris

Foraging activity in social insects should be regulated by colony nutritional status and food availability, such that both the emission of, and response to, recruitment signals depend on current conditions. Using fully automatic radio-frequency identification (RFID) technology to follow the foraging activity of tagged bumblebees (Bombus terrestris) during 16,000 foraging bouts, we tested whether the cue provided by stored food (the number of full honeypots) could modulate the response of workers to the recruitment pheromone signal. Artificial foraging pheromones were applied to colonies with varied levels of food reserves. The response to recruitment pheromones was stronger in colonies with low food, resulting in more workers becoming active and more foraging bouts being performed. In addition to previous reports showing that in colonies with low food successful foragers perform more excited runs during which they release recruitment pheromone and inactive workers are more prone to leave the nest following nectar influx, our results indicate that evolution has shaped a third pathway that modulates bumblebee foraging activity, thus preventing needless energy expenditure and exposure to risk when food stores are already high. This new feedback loop is intriguing since it involves context-dependent response to a signal. It highlights the integration of information from both forager-released pheromones (signal) and nutritional status (cue) that occurs within individual workers before making the decision to start foraging. Our results support the emerging view that responses to pheromones may be less hardwired than commonly acknowledged. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.