Energetic and time costs of foraging in harvester ants,Pogonomyrmex occidentalis

Summary Western harvester ants, Pogonomyrmex occidentalis, preferentially utilize low vegetational cover pathways. Energetic costs for foraging ants were less than 0.1% of caloric rewards of harvested seeds, suggesting that reduction of energetic cost is not a major benefit of this preference. Walking speed was significantly faster on lower cover routes, increasing net return rates from equidistant artificial food sources. Undisturbed foragers on low cover routes traveled farther, increasing their total foraging area without increasing foraging time. These results suggest that in animals with low costs of locomotion relative to energetic rewards, time costs are more important than direct energetic costs in influencing foraging decisions. In baited experiments with equidistant food sources, preferential use of low cover routes resulted in a large increase in net energetic gain rate, but only a slight increase in energetic efficiency. Under natural conditions, net energetic gain rates were constant for foragers using low and high vegetational cover routes, but foragers using low cover paths had lower efficiencies. This suggests that net energetic gain rate is a more important currency than energetic efficiency for foraging harvester ants.     

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.     

Honeybees maximize efficiency by not filling their crop

Summary Honeybees often abandon non-depleting food sources with a partially filled crop. This behaviour does not maximise the net rate of energy extraction from the food sources, and thus contradicts predictions of some common models for central place foragers. We show that including the metabolic costs of transport of nectar leads to models that predict partial crop-loading. Furthermore, the observed crop loads of honeybees are less consistent with those predicted by maximization of delivery rate to the hive (net energetic gain/ unit time), than with those predicted by maximization of energetic efficiency (net energetic gain/unit energy expenditure). We argue that maximization of energetic efficiency may be an adaptation to a limited flight-cost budget. This constraint is to be expected because a worker's condition seems to deteriorate as a function of the amount of flight performed.     

Costs of maternal care: infant-carrying in baboons

Summary Infant-carrying, the most costly form of primate parental care other than lactation, was investigated in savannah baboons of Amboseli, Kenya. Measurements of physical growth, counts and length of paces, and simultaneous records of carrying and locomotion were used to evaluate the time, distance, and energetic expenditure of infant-carrying. Finally, we modeled the energetics of independent infant locomotion and considered ontogenetic patterns in the alternative energetic costs of carrying versus independent infant locomotion under assumptions of complete nutritional dependency. The youngest infants were carried by their mothers during all travel and foraging, for a total of 8–10 km/day. By 8 months of age, both carrying time and distance were almost zero. However, daily carrying distance, unlike carrying time, did not decline in the first few months, because older infants were carried disproportionately during rapid travel and, consequently, for greater travel distances per unit carrying time. Females of low dominance rank carried their infants the most; the highest ranking mothers not only carried their infants least but biased their carrying against sons. Although carrying a growing infant is an increasingly costly behavior, during the period of nutritional dependence energetic costs to the mother are appreciably greater if an infant travels independently instead of being carried by its mother. Yet infants increased locomotor independence at a younger age than predicted by a simple model of maternal energetic efficiency. Trade-offs in energetic economy may enhance a mother's future reproduction at the expense of her present infant, may enhance survival of the present infant by promoting early acquisition of developmentally essential skills, or may suggest the importance of additional factors that influence the mother's and infant's behavior. Offprint requests to: J. Altmann     

On the integration of individual foraging strategies with colony ergonomics in social insects: nectar-collection in honeybees

Summary We experimentally tested whether foraging strategies of nectar-collecting workers of the honeybee (Apis mellifera) vary with colony state. In particular, we tested the prediction that bees from small, fast growing colonies should adopt higher workloads than those from large, mature colonies. Queenright small colonies were set up by assembling 10 000 worker bees with approximately 4100 brood cells. Queenright large colonies contained 35 000 bees and some 14 500 brood cells. Thus, treatments differed in colony size but not in worker/brood ratios. Differences in workload were tested in the context of single foraging cycles. Individuals could forage on a patch of artificial flowers offering given quantities and qualities of nectar rewards. Workers of small colonies took significantly less nectar in an average foraging excursion (small: 40.1 ± 1.1 SE flowers; large: 44.8 ± 1.1), but spent significantly more time handling a flower (small: 7.3 ± 0.4 s ; large: 5.8 ± 0.4 s). When the energy budgets for an average foraging trip were calculated, individuals from all colonies showed a behavior close to maximization of net energetic efficiency (i.e., the ratio of net energetic gains to energetic costs). However, bees from small colonies, while incurring only marginally smaller costs, gained less net energy per foraging trip than those from large colonies, primarily as a result of prolonged handling times. The differences between treatments were largest during the initial phases of the experimental period when also colony development was maximally different. Our results are at variance with simple models that assume natural selection to have shaped behavior in a single foraging trip only so as to maximize colony growth. Offprint requests to: P. Schmid-Hempel     

Colony energy requirements affect the foraging currency of bumble bees

Summary This study examines whether the foraging behavior of worker bumble bees (Bombus: Apidae) collecting nectar on inflorescences of seablush (Plectritis congesta: Valerianaceae) is affected by colony energetic requirements, which were experimentally manipulated either by adding sucrose solution to honey pots or by removing virtually all available nectar from the pots. The competing hypotheses tested were: (1) no change; energetic requirements do not affect behavior, since there is a single best way to collect food in a given environment; (2) energetic currency; the energetic currency maximized by foragers changes according to colony energetic condition, with nectar-depletion causing a shift from maximizing long-term productivity to maximizing immediate energetic gain, thereby de-emphasizing energetic costs; and (3) predation; foragers devalue risk of predation as risk of starvation increaes, with colony nectar-depletion causing foragers to be less predation riskaverse in order to increase immediate energetic gain. Relative to when their colony energy reserves were enhanced, foragers from nectar-depleted colonies selected smaller inflorescences, visited fewer flowers per inflorescence, probed flowers at a higher rate while on each inflorescence, and walked between inflorescences less often, thereby spending a greater proportion of their foraging trip in flight. These behaviors increased a bee's energetic costs while foraging, and should also have increased its immediate energetic gains, allowing rejection of the no change hypothesis. Predictions of the predation hypothesis were generally not supported, and our results best support the energetic currency hypothesis. Foraging currency of bumble bees therefore appears to be a function of colony energetic state. Offprint requests to: R.V. Cartar     

The foraging ecology of hoverflies (Diptera,Syrphidae): circular movements on composite flowers

Summary An energetic analysis of the foraging behaviour for nectar of Eristalis tenax L. is presented. The rate of energy gain while foraging on Aster is low (0.01 W) relative to similar calculations for bees, but the flies can fill their crop in about 75–220 min. Flies visit the nectar-bearing ring of florets on a capitulum systematically, leaving when they have circled it once (Fig. 1). A simple decision-making rule appears to be used to decide when to leave.     

Group size and foraging efficiency in yellow baboons

Summary I studied the foraging behaviour of adults in three different-sized groups of yellow baboons (Papio cynocephalus) at Amboseli National Park in Kenya to assess the relationship between group size and foraging efficiency in this species. Study groups ranged in size from 8 to 44 members; within each group, I collected feeding data for the dominant adult male, the highest ranking pregnant female, and the highest ranking female with a young infant. There were no significant differences between groups during the study in either the mean estimated energy value of the food ingested per day for each individual (385±27 kJ kg^-1 day^-1) or in the estimated energy expended to obtain that food (114±3 kJ kg^-1 day^-1). Mean foraging efficiency ratios, which reflect net energy gain per unit of foraging time, also did not vary as a function of the size of the group in which the baboons were living. There was substantial variation between days in the efficiency ratios of all animals; this was the result of large differences in energy intake rather than in the energy expended during foraging itself. The members of the smallest group spent on the average only one-half as much time feeding each day as did individuals in the two larger groups. However, they obtained almost as much energy while foraging, primarily because their rate of food intake while actually eating tended to be higher than the rate in the other groups. The baboons in the small group were observed closer to trees that they could climb to escape ground predators, and they also were more likely to sit in locations elevated above the ground while resting. Such differences would be expected if the members of the small group were less able to detect approaching predators than individuals that lived in the larger groups. The results of this study suggest that predator detection or avoidance, rather than increased foraging efficiency, may be the primary benefit of living in larger groups in this population.     

Seasonal changes in foraging strategies of nesting blackbirds (Turdus merula L.)

Summary Blackbirds are usually multiple-prey loaders and forage mainly on the ground. We analysed the foraging behaviour of ten males in an urban park in Budapest during the breeding season from 1984 to 1986. At the end of April and in May blackbirds fed their nestlings mainly on earthworms (load type I). In this period the average scarching time and route were shorter, and the territories of the pairs tended to be smaller, than in June, when males in addition brought a great variety of invertebrates per load (load type II) to the young. The average dry weight and energy content of the two load types did not differ significantly. However, the average energy delivery rate (energy content/intervisiting time) and rate of energy gain (energy content/searching time) were higher when males collected earthworms, because intervisiting and searching times were shorter. The frequency distribution of searching times for load type I suggests that the encounter with earthworms was random. For load type II birds seemed to employ a fixed-mass foraging strategy. In June, the drier conditions reduced the availability of earthworms, and blackbirds extended their foraging areas.     

Self-organization in collective honeybee foraging: emergence of symmetry breaking,cross inhibition and equal harvest-rate distribution

De Vries and Biesmeijer described in 1998 an individual-oriented model that simulates the collective foraging behaviour of a colony of honeybees. Here we report how this model has been expanded and show how, through self-organization, three colony-level phenomena can emerge: symmetry breaking, cross inhibition and the equal harvest-rate distribution. Symmetry breaking is the phenomenon that the numbers of foragers visiting two equally profitable food sources will diverge after some time. Cross inhibition is the phenomenon that, by increasing the profitability of one of two equal food sources, the number of foragers visiting the other source will decrease. In some circumstances, the bees foraging on two sources of different profitabilities will be distributed between these sources such that the two average energy harvest rates are equal. We will refer to this phenomenon as the equal harvest-rate distribution. For each of these three phenomena, we show what the necessary behavioural rules to be followed by the individual forager bees are, and what the necessary circumstances are (that is, what values the model parameters should take) in order for these phenomena to arise. It seems that patch size and forager group size largely determine when each of these phenomena will arise. Experimenting with two types of currency, net gain rate and net gain efficiency, revealed that only gain rate may result in an equal harvest-rate distribution of foragers visiting different food sources.     

Costs and benefits of pocket gopher foraging: linking behavior and physiology

Animals can attain fitness benefits by maintaining a positive net energy balance, including costs of movement during resource acquisition and the profits from foraging. Subterranean rodent burrowing provides an excellent system in which to examine the effects of movement costs on foraging behavior because it is energetically expensive to excavate burrows. We used an individual-based modeling approach to study pocket gopher foraging and its relationship to digging cost, food abundance, and food distribution. We used a unique combination of an individual-based foraging-behavior model and an energetic model to assess survival, body mass dynamics, and burrow configurations. Our model revealed that even the extreme cost of digging is not as costly as it appears when compared to metabolic costs. Concentrating digging in the area where food was found, or area-restricted search (ARS), was the most energetically efficient digging strategy compared to a random strategy. Field data show that natural burrow configurations were more closely approximated by the animals we modeled using ARS compared to random diggers. By using behavior and simple physiological principles in our model, we were able to observe realistic body mass dynamics and recreate natural movement patterns.     

The choice of two prey types that minimises the probability of starvation

Summary In this paper we investigate the optimal diet of a forager faced with two prey types. Classical optimal foraging theory, based on the maximization of the mean net rate of energetic gain , predicts that the optimal policy is either to take only the more profitable prey type or to take both prey types. The decision between these policies does not depend on the forager's energy reserves or the time available for foraging. We develop two alternative models, based on the minimization of the probability of starvation. In the first model, foraging occurs continuously, and it is optimal to take a prey type if and only if it increases the forager's energy reserves. In the second model foraging stops at dusk, and the forager dies during the night if its reserves at dusk are too low. The optimal policy, which has to be found numerically by dynamic programming, depends on the forager's reserves and the time left till dusk. In general the optimal policy is either to take both types or to take only the more profitable type. Taking both types is optimal when reserves are low, and there is some evidence that this occurs. The models show that factors that have been ignored in classical models may be of importance.     

Net energy versus efficiency maximizing by foraging ring-billed gulls

Summary Ring-billed gulls (Larus delawarensis) breeding at Dog Lake, Manitoba often feed by following tractors pulling cultivating implements around fields. Tractor-following gulls always land immediately behind the cultivating implement, where they feed on earthworms or grain. Afeer a feeding bout on the ground (patch residence time), gulls fly up, pursue the tractor and repeat the cycle. We use net energy maximizing (energy gained per unit time) and efficiency maximizing (energy gained per unit energy expended) models to make quantitative predictions of patch residence time, and compare these predictions to observations. If we assume flight speed to be constrained at the observed mean, the observations fall between the predictions of the two models, and the models explain approximately equal and highly significant proportions of the overall variation in patch residence time. If both flight speed and patch residence time are allowed to vary in the models, the efficiency maximizing model more closely predicts observed patch residence times, and the net energy maximizing model more closely predicts observed flight speeds. We discuss whether breeding ringbilled gulls may be truly intermediate between net energy and efficiency maximizing, and how measurements of flight speed may be useful in further investigations.     

Prey caloric value and predator energy needs: foraging predictions for wild spinner dolphins

Spinner dolphins (Stenella longirostris) feed on individual small (2–10 cm long) prey that undergo diel vertical migrations, presumably making them inaccessible to dolphins during the day. To examine how time, prey behavior, prey distribution, and energy needs constrain dolphin foraging, a calorimeter was used to measure the caloric content of prey items. These data were combined with information on prey distribution in the field and the energetic needs of dolphins to construct basic bioenergetic models predicting the total prey consumption and mean feeding rates of wild dolphins as well as potential prey preferences. The mean caloric density of mesopelagic animals from Hawaii was high (2,837 cal/g wet weight for shrimps, squids, and myctophid fishes). Their total caloric content, however, was low because of their small size. Energy value of prey and energetic needs of spinner dolphins were used to examine the effect of time and energy constraints on dolphin foraging. The results predict that spinner dolphins need to consume an estimated minimum of 1.25 large prey items per minute to meet their maintenance energy needs. If the additional energy costs of foraging are considered, the estimated necessary foraging rate is predicted to increase only slightly when large prey are consumed. If smaller prey are consumed, the total energy demand may be twice the basic maintenance value. Prey density and size are predicted to be important in determining if dolphins can forage successfully, meeting their energetic needs. The prey size predictions compare well with results from previous gut content studies and from stomach contents of a recently stranded spinner dolphin that had enough prey in its stomach to meet its estimated basic maintenance energy needs for a day. Finally, the results suggest that spinner dolphins are time and therefore efficiency limited rather than being limited by the total amount of available prey. This may explain the diel migration exhibited by spinner dolphins that allows them to follow the movements of their prey and presumably maximizes their foraging time.Communicated by P.W. Sammarco, Chauvin     

Effects of energy requirements and worker mortality on colony growth and foraging in the honey bee

Summary A model of colony growth and foraging in the honey bee (Apis mellifera L.) is presented. It is assumed that summer workers choose a foraging strategy that maximizes colony population by the end of the season subject to the constraint that enough nectar has been stored to sustain the adult population overwinter. The optimal foraging strategy is derived with respect to the number of flowers visited during one foraging trip. A forager that visits many flowers collects a substantial amount of nectar but the probability that the worker returns alive from the excursion decreases accordingly. Using dynamic modelling, I explore the effects on colony growth of colony population, colony energy requirements and mortality rate while foraging. The model shows that when the expected rate of increase in nectar reserves is low, for instance in small colonies or when mortality rate rises rapidly with foraging intensity, workers collect more nectar during each foraging trip. The increase in foraging activity is realized at the expense of colony growth. The main finding is that depending on colony status the foraging strategy that maximizes worker population implies visits to almost any number of flowers. This is in sharp contrast to predictions from traditional foraging models where foraging intensity is assumed to cluster around values that maximize net rate or efficiency. The model suggests that strategies that cluster around rate and efficiency maximization should be viewed as particular solutions to a more general problem.     

Temporal variability in winter travel patterns of Yellowstone bison: the effects of road grooming.

The influence of winter recreation on wildlife in Yellowstone National Park (YNP), Wyoming and Montana, USA, is a controversial issue. In particular, the effects of road grooming, done to facilitate snowmobile and snowcoach travel, on bison (Bison bison) ecology are under debate. We collected data during winters, from 1997 to 2005, on bison road use, off-road travel, and activity budgets to quantify temporal trends in the amount of bison road and off-road travel and to identify the ecological factors affecting bison movements and use of the groomed road system in the Madison-Gibbon-Firehole (MGF) area of YNP. Using model comparison techniques, we found bison travel patterns to be influenced by multiple, interacting effects. Road travel was negatively correlated with road grooming, and we found no evidence that bison preferentially used groomed roads during winter. Snow water equivalent, bison density, and the springtime melt period were positively correlated with both bison road and off-road travel. From behavioral scans on 68,791 bison, we found that travel is only a small percentage (11%) of all bison activity, with foraging comprising 67% of observations. Also, only 7% of traveling bison and 30% of foraging bison were displacing snow, and we suggest foraging, rather than traveling, is likely the major energetic cost to bison in winter. Bison utilize their own trail network, connecting foraging areas using stream corridors, geothermal pathways, and self-groomed travel routes. Our results indicate that temporal patterns in bison road travel are a manifestation of general travel behavior and that groomed roads in the MGF do not appear to be a major factor influencing bison ecology and spatial redistribution. We suggest that the changes in bison spatial dynamics during the past three decades have likely been the result of the natural phenomenon of density-dependent range expansion, rather than having been caused by the anthropogenic influence of road grooming.     

Why are bumble bees risk-sensitive foragers?

Summary In a controlled laboratory experiment, we re-examined the question of bumble bee risk-sensitivity. Harder and Real's (1987) analysis of previous work on bumble bee risk aversion suggests that risk-sensitivity in these organisms is a result of their maximizing the net rate of energy return (calculated as the average of expected per flower rates). Whether bees are risk-sensitive foragers with respect to minimizing the probability of energetic shortfall is therefore still an open question. We examined how the foraging preferences of bumble bees for nectar reward variation were affected by colony energy reserves, which we manipulated by draining or adding sucrose solution to colony honey pots. Nine workers from four confined colonies of Bombus occidentalis foraged for sucrose solution in two patches of artificial flowers. These patches yielded the same expected rate of net energy intake, but floral volumes were variable in one patch and constant in the other. Our results show that bumble bees can be both risk-averse (preferring constant flowers) and risk-prone (preferring variable flowers), depending on the status of their colony energy reserves. Diet choice in bumble bees appears to be sensitive to the target value a colony-level energetic requirement. Offprint requests to: R.V. Cartar     

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.     

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.     

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.