Assessment of food source profitability in honeybees (<Emphasis Type="Italic">Apis mellifera</Emphasis>): how does disturbance of foraging activity affect trophallactic behaviour?

When forager honeybees (Apis mellifera) return to the hive after a successful foraging trip, they unload the collected liquid to recipient hive mates through mouth-to-mouth contacts (trophallaxis). The speed at which the liquid is transferred (unloading rate) from donor to recipient is related to the profitability of the recently visited food source. Two main characteristics that define this profitability are the flow of solution delivered by the feeder and the time invested by the forager at the source (visit time). To investigate the effect of visit time on trophallactic behaviour, donor foragers were trained to a rate feeder that could deliver different flows of solution. We dissociated visit time and flow of solution by introducing pauses in the solution's deliverance at different moments of the foraging visit. We analysed whether timing of the non-deliverance period within the visit is important for the forager's assessment of resource profitability. During the subsequent trophallactic encounter with a hive mate, unloading rate was related to the total time invested by the forager at the food source only if the ingestion process had already been started. These results together with previous ones suggest that foragers integrate an overall flow rate of solution of the feeder throughout the entire foraging visit.     

Sticking to their choice – honey bee subfamilies abandon declining food sources at a slow but uniform rate

Abstract. 1. The allocation of honey bee foragers among food patches is a result of decisions made by individual bees that are based on internal and external cues.
2. Decision-making processes are often based on internal thresholds. For example, if the quality of the food source is assessed by a forager as exceeding its internal threshold, the bee will continue foraging on that food source.
3. It is often assumed that all individuals have the same threshold and therefore use the same thresholds in decision-making, but because the honey bee queen mates with 12–30 males, the workers within a colony are genetically heterogeneous. Thus, the thresholds used by individual bees may be genetically variable within a colony.
4. Models of colony-level foraging behaviour of honey bees suggest that the rate of abandoning food sources is a critical parameter affecting foraging success. Moreover, these models show that variance among subfamilies in their abandonment rates may increase the colony's foraging efficiency.
5. Experimental data showing the relationship between the probability of abandoning a food source and its profitability are lacking, as is information on any variation in abandonment rates among subfamilies.
6. Abandonment rates were determined experimentally for four honey bee families for seven different sucrose concentrations. The results showed that abandonment rates appear to be invariant among (sub)families. The importance of forager fidelity to declining food sources is discussed with respect to foraging efficiency in a changing environment.     

Interactions with Combined Chemical Cues Inform Harvester Ant Foragers' Decisions to Leave the Nest in Search of Food

Social insect colonies operate without central control or any global assessment of what needs to be done by workers. Colony organization arises from the responses of individuals to local cues. Red harvester ants (Pogonomyrmex barbatus) regulate foraging using interactions between returning and outgoing foragers. The rate at which foragers return with seeds, a measure of food availability, sets the rate at which outgoing foragers leave the nest on foraging trips. We used mimics to test whether outgoing foragers inside the nest respond to the odor of food, oleic acid, the odor of the forager itself, cuticular hydrocarbons, or a combination of both with increased foraging activity. We compared foraging activity, the rate at which foragers passed a line on a trail, before and after the addition of mimics. The combination of both odors, those of food and of foragers, is required to stimulate foraging. The addition of blank mimics, mimics coated with food odor alone, or mimics coated with forager odor alone did not increase foraging activity. We compared the rates at which foragers inside the nest interacted with other ants, blank mimics, and mimics coated with a combination of food and forager odor. Foragers inside the nest interacted more with mimics coated with combined forager/seed odors than with blank mimics, and these interactions had the same effect as those with other foragers. Outgoing foragers inside the nest entrance are stimulated to leave the nest in search of food by interacting with foragers returning with seeds. By using the combined odors of forager cuticular hydrocarbons and of seeds, the colony captures precise information, on the timescale of seconds, about the current availability of food.     

The ontogeny of foragwehaviour in desert ants, Cataglyphis bicolor

Abstract. 1. Individually foraging desert ants, Cataglyphis bicolor , exhibit short foraging lives (half lifetime, i.e. half-time of the exponential decay function: 4.5 days), in which they perform 3.7 ± 1.9 foraging runs per day.
2. During their short lifetime foraging period the ants increase the duration of their foraging round trips (up to 40.0 ± 24.6 min per run), the maximal distance of individual foraging runs (up to 28.2 ± 4.1 m), and their foraging success, i.e. the ratio of successful runs to the total number of runs (up to 0.70).
3. The parameter that increases most dramatically during a forager's lifetime is direction fidelity, i.e. the tendency to remain faithful to a particular foraging direction.
4. A model based on some simple behavioural rules is used to describe the experimental findings that within an isotropic food environment individual ants develop spatial foraging idiosyncrasies, and do so at a rate that increases with the food densities they encounter.
5. Finally, it is argued that in functional terms direction fidelity is related to the navigational benefits resulting from exploiting familiar (route-based) landmark information, and hence reduces round-trip time and by this physiological stress and predatory risk.     

The glass is half-full: overestimating the quality of a novel environment is advantageous

According to optimal foraging theory, foraging decisions are based on the forager's current estimate of the quality of its environment. However, in a novel environment, a forager does not possess information regarding the quality of the environment, and may make a decision based on a biased estimate. We show, using a simple simulation model, that when facing uncertainty in heterogeneous environments it is better to overestimate the quality of the environment (to be an "optimist") than underestimate it, as optimistic animals learn the true value of the environment faster due to higher exploration rate. Moreover, we show that when the animal has the capacity to remember the location and quality of resource patches, having a positively biased estimate of the environment leads to higher fitness gains than having an unbiased estimate, due to the benefits of exploration. Our study demonstrates how a simple model of foraging with incomplete information, derived directly from optimal foraging theory, can produce well documented complex space-use patterns of exploring animals.     

The influence of snow on the functional response of grazing ungulates

The forage intake rate of grazing ungulates is limited either by the rate at which they encounter food items, or the rate at which food items are handled. Whether an ungulate is encounter‐ or handling‐limited influences spatial and temporal depletion of forage, daily time budgets, and ultimately animal condition. Previously, vegetation abundance has been used as a surrogate for an ungulate's encounter rate with food items and related to observed bite rate to determine whether intake rate is encounter‐ or handling‐limited. In temperate climates snow accumulation during winter limits access to vegetation by forcing animals to wade and paw through snow to consume underlying vegetation, increasing the amount of time required to encounter a food item. As a result, an ungulate may be handling‐limited when foraging in a high biomass system under snow‐free conditions, but becomes encounter‐limited when snow accumulates. We derived a model that provides a frame work for estimating the rate at which a grazing ungulate encounters vegetation by considering foraging velocity, vegetation biomass and the time required to paw away snow when present. We then used data from focal observations of 36 wild elk Cervus canadensis wintering on a montane grassland in the Canadian Rockies of Alberta, Canada, to apply our model and estimate encounter rate over a range of vegetation abundance and snow conditions. Using AIC_c in a model selection approach we found that an asymptotic regression model of observed bite rate as a function of estimated encounter rate provided a better fit than similar models using only vegetation abundance as the explanatory variable. An asymptotic model suggests elk were handling‐limited in the absence of snow, but became encounter‐limited when snow accumulated. Our results demonstrate the importance of considering the influence of factors other than vegetation abundance on the intake rate of grazing ungulates.     

Harvest rates and foraging strategies in Negev Desert gerbils

We examined the foraging strategy and quantified the foragingtraits of two nocturnal rodent species, Allenby's gerbil (Gerbillusallenbyi) and the greater Egyptian sand gerbil (Gerbillus pyramidum).In the laboratory, both species used two distinct foragingstrategies: either they immediately consumed seeds found ina patch (seed tray); or they collected and delivered the seedsto their nest box for later consumption. Moreover, we founda transition in foraging strategy among individual G. allenbyi under laboratory conditions; they all began by consuming theseeds on the tray and, after 7 days on average, switched tothe collecting strategy. By contrast, in the field both speciesused only one foraging strategy; they collected and deliveredthe seeds to their burrow or to surface caches for later consumption.Furthermore, G. allenbyi and G. pyramidum collected seeds atsignificantly higher rates in the field than in the laboratorybecause the seed encounter rates for both species were higherin the field. This suggests that in natural conditions, probablyinvolving predation risk and competitive pressure, gerbilsmust respond in two ways: (1) they must choose a foraging strategythat reduces predation risk by minimizing time spent feedingoutside their burrows; and (2) they must forage more efficiently.In the field, seed handling time of the larger species, G. pyramidum, was shorter than that of the smaller one, G. allenbyi.This difference may give G. pyramidum an advantage when resourcelevels are high and when most of a forager's time is spent handling seeds rather than searching for more seeds. Additionally,our field study showed that the seed encounter rate of G. allenbyiwas higher than that of G. pyramidum. This difference may giveG. allenbyi an advantage when resource levels are low and whensearching occupies most of the forager's time. The differentadvantages that each species has over the other, under differentconditions, may well be factors promoting their coexistenceover a wide range of resource densities.     

The foraging benefits of information and the penalty of ignorance

Patch use theory and the marginal value theorem predict that a foraging patch should be abandoned when the costs and benefits of foraging in the patch are equal. This has generally been interpreted as all patches being abandoned when their instantaneous intake rate equals the foraging costs. Bayesian foraging – patch departure is based on a prior estimate of patch qualities and sampling information from the current patch – predicts that instantaneous quitting harvest rates sometimes are not constant across patches but increase with search time in the patch. That is, correct Bayesian foraging theory has appeared incompatible with the widely accepted cost–benefit theories of foraging. In this paper we reconcile Bayesian foraging with cost–benefit theories. The general solution is that a patch should be left not when instantaneous quitting harvest rate reaches a constant level, but when potential quitting harvest rate does. That is, the forager should base its decision on the value now and in the future until the patch is left. We define the difference between potential and instantaneous quitting harvest rates as the foraging benefit of information, FBI. For clumped prey the FBI is positive, and by including this additional benefit of patch harvest the forager is able to reduce its penalty of ignorance.     

Consumer-food systems: why type I functional responses are exclusive to filter feeders

The functional response of a consumer is the relationship between its consumption rate and the abundance of its food. A functional response is said to be of type I if consumption rate increases linearly with food abundance up to a threshold level at which it remains constant. According to conventional wisdom, such type I responses are more frequent among filter feeders than among other consumers. However, the validity of this claim has never been tested. We review 814 functional responses from 235 studies, thereby showing that type I responses are not only exceptionally frequent among filter feeders but that they have only been reported from these consumers. These findings can be understood by considering the conditions that a consumer must fulfil in order to show a type I response. First, the handling condition: the consumer must have a negligibly small handling time (i.e. the time needed for capturing and eating a food item), or it must be able to search for and to capture food while handling other food. Second, the satiation condition: unless its gut is completely filled and gut passage time is minimal, the consumer must search for food at a maximal rate with maximal effort. It thus has to spend much time on foraging (i.e. searching for food and handling it). Our functional response review suggests that only filter feeders sometimes meet both of these conditions. This suggestion is reasonable because filter feeders typically fulfil the handling condition and can meet the satiation condition without losing time, for they are, by contrast to non-filter feeders, able simultaneously to perform foraging and non-foraging activities, such as migration or reproduction.     

Honeybees assess changes in nectar flow within a single foraging bout

Forager honeybees returning to the hive after a successful foraging trip unload the collected liquid to recipient hivemates through mouth-to-mouth food exchange contacts (trophallaxis). The speed at which the liquid is transferred (unloading rate) from donor to recipient is related to the profitability offered by the recently visited food source. Two of the main characteristics that define food source profitability are the flow of solution delivered by the feeder and the time invested by the forager feeding at the source (feeding time). To investigate which of these two variables is related to unloading rate, we individually trained donor foragers to a regulated-flow feeder that presented changes in the delivered flow of solution within a single foraging bout, while feeding time remained constant. With the range of flows used, bees attained maximum crop loads in all experiments. During the subsequent trophallactic encounter with an unfed recipient hivemate, unloading rate was differentially affected by the changes in flow of solution presented during the previous foraging trip at the source, depending on whether there had been an increase or a decrease of flow rate within that visit. Foragers unloaded at lower rates when they experienced a decrease in flow rate, but did not increase the unloading rate when presented with an increase at the food source. Thus, forager honeybees seem to be able to detect variations in the delivered flow of solution, since they modulate unloading rate in relation to these changes, although decreases in food value seem to be perceptually weighted in relation to increases, independently of the time invested in the food-gathering process.     

Fast food in ant communities: how competing species find resources

An understanding of foraging behavior is crucial to understanding higher level community dynamics; in particular, there is a lack of information about how different species discover food resources. We examined the effect of forager number and forager discovery capacity on food discovery in two disparate temperate ant communities, located in Texas and Arizona. We defined forager discovery capacity as the per capita rate of resource discovery, or how quickly individual ants arrived at resources. In general, resources were discovered more quickly when more foragers were present; this was true both within communities, where species identity was ignored, as well as within species. This pattern suggests that resource discovery is a matter of random processes, with ants essentially bumping into resources at a rate mediated by their abundance. In contrast, species that were better discoverers, as defined by the proportion of resources discovered first, did not have higher numbers of mean foragers. Instead, both mean forager number and mean forager discovery capacity determined discovery success. The Texas species used both forager number and capacity, whereas the Arizona species used only forager capacity. There was a negative correlation between a species’ prevalence in the environment and the discovery capacity of its foragers, suggesting that a given species cannot exploit both high numbers and high discovery capacity as a strategy. These results highlight that while forager number is crucial to determining time to discovery at the community level and within species, individual forager characteristics influence the outcome of exploitative competition in ant communities.     

Central place foraging in larvae of the charaxine butterfly,Polyura pyrrhus (L.): A case study in a herbivore

Central place foraging by larvae of the charaxine butterfly,Polyura pyrrhus, was studied. Larvae made foraging trips from the silken pads they constructed on leaflets of their foodplant,Acacia sp. A foraging trip sometimes involved complete depletion of a single patch of foodplant pinnules. Larvae which did not deplete a patch appeared to eat until they were satiated, whereas larvae which depleted a patch either visited another patch (multiple-patch foraging) or returned directly to the pad (single-patch foraging). If the food intake at the first patch was small a larva tended to make a “multiple-patch” decision, especially when the pinnule-patch was distant from the resting pad. The duration between successive foraging trips (resting time on the pad) was much longer than the round trip duration: on average about 3 h and 15 min, respectively. The resting time is suggested to be a handling time (i.e., digesting food in the gut) and was disproportional to the amount of food consumed, i.e., the handling efficiency was higher when the larva consumed a larger amount of food. This may be the reason why larvae usually ate until they were satiated. A food-intake-rate maximizing model was constructed to describe the decision rule as to whether a larva should make a single-patch or a multiple-patch foraging trip. One of the model's predictions (i.e., larvae should engage in multiple-patch foraging when the food intake at the first patch is small) qualitatively corresponds with data, however, the model does not explain the effect of travelling time on decision making in larvae. Several other factors which may influence the decision making of larvae are discussed.     

The short-term regulation of foraging in harvester ants

In the seed-eating ant Pogonomyrmex barbatus, the return ofsuccessful foragers stimulates inactive foragers to leave thenest. The rate at which successful foragers return to the nestdepends on food availability; the more food available, the morequickly foragers will find it and bring it back. Field experimentsexamined how quickly a colony can adjust to a decline in therate of forager return, and thus to a decline in food availability,by slowing down foraging activity. In response to a brief, 3-to 5-min reduction in the forager return rate, foraging activityusually decreased within 2–3 min and then recovered within5 min. This indicates that whether an inactive forager leavesthe nest on its next trip depends on its very recent experienceof the rate of forager return. On some days, colonies respondedmore to a change in forager return rate. The rapid colony responseto fluctuations in forager return rate, enabling colonies toact as risk-averse foragers, may arise from the limited intervalover which an ant can track its encounters with returning foragers.     

Mean-variance sets for dietary choice models: simplicity in a complex world

Summary This paper presents a series of simulations designed to determine optimal diet breadth under shortfall avoidance models. Profitability and encounter rate functions were varied, and means and variances of energy intake rate were generated using a simple simulation procedure. The resulting mean-variance sets assumed three distinct shapes: u-shaped, arched, and looped. These simulations show that certain mean-variance sets allow the forager to employ simple behavioural rules to determine the optimal diet breadth. This situation occurs when low ranking diet items have small handling times, and these conditions may be quite common. In other cases, mean-variance sets may be too complicated to allow for easy behavioural rules designed to minimize starvation probability. The ability to characterize foraging problems into a limited series of mean-variance set types benefits workers examining the evolution and maintenance of foraging strategies, since these sets have clear implications for the ability of animals to develop simple behavioural rules. Unfortunately data are lacking on the profitability and encounter rate distributions animals face in nature.     

A simple rule for the costs of vigilance: empirical evidence from a social forager

It is commonly assumed that anti-predator vigilance by foraging animals is costly because it interrupts food searching and handling time, leading to a reduction in feeding rate. When food handling does not require visual attention, however, a forager may handle food while simultaneously searching for the next food item or scanning for predators. We present a simple model of this process, showing that when the length of such compatible handling time Hc is long relative to search time S, specifically Hc/S > 1, it is possible to perform vigilance without a reduction in feeding rate. We test three predictions of this model regarding the relationships between feeding rate, vigilance and the Hc/S ratio, with data collected from a wild population of social foragers (samango monkeys, Cercopithecus mitis erythrarchus). These analyses consistently support our model, including our key prediction: as Hc/S increases, the negative relationship between feeding rate and the proportion of time spent scanning becomes progressively shallower. This pattern is more strongly driven by changes in median scan duration than scan frequency. Our study thus provides a simple rule that describes the extent to which vigilance can be expected to incur a feeding rate cost.     

Downy woodpecker foraging behavior: foraging by expectation and energy intake rate

Summary I describe an artificial patch system that was used to study the foraging behavior of free-roaming downy woodpeckers (Picoides pubescens) in a woodlot in southeastern Michigan. The artificial patches used were thin logs into which were drilled small holes to hold food items (bits of sunflower seed kernels). Downy woodpeckers would systematically search the holes of a patch for food items and thus by manipulating the food distribution within the patches, the birds could be made to experience differing rates of energy intake while foraging.Simple deterministic theories of optimal foraging in patchy environments indicate that an optimal forager, who experiences a decreasing rate of energy intake while foraging in a patch, should leave a patch when its rate of energy intake falls below the average intake rate for the overall environment. In other words, an optimal forager is continually assessing the quality of a patch and makes decisions as to when to leave a patch via its energy intake rate. When the downy woodpeckers studied could encounter any one of several types of patches each with differing, decreasing rates of energy intake, they followed a patch quality assessment strategy similar to that suggested by theory. Upon encountering a single type of patch for a number of consecutive days, however, the birds appeared to forage according to prior expectations of patch quality and not according to a quality assessment strategy based on energy intake rates. The observed expectations were not related to the number of food items per patch but they appeared to be based on expectations of when or where to leave a patch.     

The consequences of partially directed search effort

Search effort is undirected when a forager has a stereotypical searching behaviour that results in fixed encounter rates with its prey (e.g. diet choice models), and is directed when the forager can bias its encounter with a ‘chosen’ prey. If the bias is complete, search is totally directed (e.g. habitat selection models). When the bias is incomplete (i.e. search modes are not exclusive to a single prey type), search is partially directed. The inclusion of a prey type in the diet is then the result of two decisions: (1) which prey to search for and (2) which prey to handle. The latter decision is determined by the ratio of energy to handling time and the abundance of the preferred prey. The former decision is a function of the encounter probabilities and densities of all potential prey types in addition to their ratio of energy to handling time. Assuming two prey types, there are three distinct behavioural strategies: (1) search for the preferred prey/forage selectively; (2) search for the preferred prey/forage opportunistically; and (3) search for the non-preferred prey/forage opportunistically. If prey are depletable (i.e. prey occur in resource patches), the forager may switch search modes such that prey are depleted to the point where the marginal values of the search modes are equalized. This revised version was published online in July 2006 with corrections to the Cover Date.     

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.     

Optimal foraging: the difficulty of exploiting different feeding strategies simultaneously

Summary The foraging efficiency of a visually feeding fish, perch (Perca fluviatilis) was studied on two prey species (Daphnia magna and Chaoborus obscuripus) presented either separately or combined. It is shown that when both prey species are present, the foraging efficiency of the predator is reduced. This is due to the predator's inability to simultaneously cope with prey species with different anti-predatory behaviour. In the mixed-meal experiment the predator captured both prey species in equal proportions in disagreement with optimal foraging models assuming that handling time and encounter rate for a prey species are independent of other prey species. The results are, however, in agreement with optimal foraging models assuming that handling time and encounter rate are influenced by short time learning.     

Intake rate at differently scaled heterogeneous food distributions explained by the ability of tactile-foraging mallard to concentrate foraging effort within profitable areas

The ability to respond to spatial heterogeneity in food abundance depends on the scale of the food distribution and the foraging scale of the forager. The aim of this study is to illustrate that a foraging scale exists, and that at larger scaled food distributions foragers benefit from the ability to subdivide a continuous (non-discrete) heterogeneous environment into profitable and non-profitable areas. We recorded search patterns of mallards Anas plathyrhynchos foraging in shallow water on cryptic prey items (millet seeds), distributed at different scales. A small magnet attached to the lower mandible allowed us to record in great detail the position and movements of the bill tip within a feeding tray underlain by magnet sensors. Instantaneous intake rate was determined in a subsequent experiment. We successfully determined the foraging scale (about 2×2 cm), defined as the scale above which foragers do respond (coarse scaled distribution) and below which foragers do not respond (fine scaled distribution) to spatial heterogeneity, by concentrating foraging effort within areas of high food density. A response resulted in a significantly higher intake rate, compared to a homogeneous distribution with an equal overall density. Unlike systematic search cell revisitation was common in trials, and at coarse scaled food distributions even slightly (but significantly) more frequently observed than predicted for random search. Mallards respond to food capture by restricting displacement (area restricted search) at food distributions that are considered to be clumped for the forager (large scaled coarse distributions). We argue that partitioning the environment at the foraging scale in itself could be a mechanism to concentrate foraging efforts within profitable areas, because mallard were able to respond to heterogeneity at coarse scaled food distributions even when non-clumped (i.e. without conducting area restricted search).