Choice and context: testing a simple short-term choice rule

Psychological studies of animal choice show that the immediate consequences of choice strongly influence preference. In contrast, evolutionary models emphasize the longer-term fitness consequences of choice. Building on recent work by Stephens & Anderson (2001, Behavioral Ecology12, 330-339), this study presents two experiments that address this conflict. Stephens & Anderson developed an alternative choice situation based on patch-leaving decisions and compared this to the binary choice, or self-control, situation typically used in psychological studies. They hypothesized that the same short-term choice rule could account for choice in both situations, maximizing long-term gains in the patch situation, but typically producing shortsighted results in the self-control case. Experiment 1 used captive blue jays, Cyanocitta cristata, to test this ‘same rule’ hypothesis. The results do not support this hypothesis, suggesting that if a single rule applies, it is probably a more complex rule. Stephens & Anderson also hypothesized that a rule based on the delay to the next meal could explain why the intertrial interval has little effect in binary choice studies, even though the analogous travel time strongly affects patch-leaving decisions. When an animal leaves a patch, it experiences a delay consisting of the travel time plus time spent searching in the patch until food is obtained. Experiment 2 tested the hypothesis that travel time and search time combine additively, behaving like a single delay. Using treatments that created the same combined delay via different combinations of travel and search time, we found no evidence of nonadditivity, suggesting that these two components may indeed be treated as a single delay. Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.      

Maximizing feeding efficiency and minimizing time exposed to predators: a trade-off in the black-capped chickadee

Summary Animals often must feed away from protective cover, sometimes at a considerable risk of being preyed upon. Feeding at the maximum rate while away from cover may simultaneously minimize the time spent exposed to predators, but this is not always the case. Under some circumstances, carrying prey items to protective cover before they are consumed will minimize the time spent exposed to predators, whereas feeding at maximum efficiency (staying to eat prey where they are found) will actually increase the time spent exposed to predators. Whether or not there is a conflict between maximizing foraging efficiency and minimizing exposure time, depends upon the travel time to cover relative to the handling time of a prey item; short handling times and/or long travel times are associated with the no-conflict situation, whereas the conflict situation is associated with long handling times and/or short travel times to cover. Free-ranging chickadees foraging at an artificial patch at various distances from cover can distinguish between these two foraging situations. When there is no conflict, they stay and eat at the patch. Their behavior in the conflict situation indicates that they are tradingoff foraging considerations against the risk of predation. When the cost of carrying is low and the benefit gained is high, the chickadees elect to carry items to cover; they tend to stay and eat at the patch when the relative magnitudes of costs and benefits are reversed.     

Florida Scrub-Jays (Aphelocoma coerulescens) are Sentinels More When Well-Fed (Even with no Kin Nearby)

Sentinels occupy high, exposed positions while other group members forage nearby. If sentinel behavior involves a foraging–predation risk trade‐off, animals should be sentinels more when fed supplemental food. When individual Florida scrub‐jays (Aphelocoma coerulescens) were fed fragments of peanuts, during the following 30 min they shifted 30% of their time from foraging to sentinel behavior. In a follow‐up experiment, we fed either one or two members in each group. As before, the jays reduced their foraging and spent much more time as sentinels when given supplemental food. In each treatment, pairs were sentinels simultaneously considerably less often than expected by chance. The dramatic shift from foraging to sentinel behavior suggests that for Florida scrub‐jays sentinel behavior brings substantial benefits for no greater cost than that of lost opportunities to forage. Because the results held for simple mated pairs of scrub‐jays, we argue that kin selection and social prestige are not necessary to explain sentinel behavior.     

Why do animals make better choices in patch-leaving problems?

This study compares two procedures for the study of choices that differ in time and amount, namely the self-control and patch procedures. The self-control procedure offers animals a binary mutually exclusive choice between a smaller–sooner and larger–later option. This procedure dominates the choice literature. It seems to address the idea of choice in a general, but relatively abstract way. Animals in the self-control situation frequently prefer the smaller–sooner option even when the larger–later option yields a higher long-term intake rate. In contrast, the patch procedure poses an economically similar question, but simulates the naturally occurring problem of patch exploitation. In the patch procedure, animals choose between leaving and staying. Emerging evidence suggests that animals perform better and achieve higher long-term intake rates in the patch situation. This observation raises the question of how a single set of choice mechanisms could produce these different outcomes. The experiment presented here tests two hypotheses about the relationship between the patch and self-control situations. First, it asks whether the short-term rate rule can predict choice behavior in both situations. Second, it tests the second-delivery hypothesis which holds that the patch situation favors choosing the larger more delayed option (staying) because this option ultimately leads to two food deliveries. The results of this experiment convincingly reject both of these hypotheses. Indeed, our results suggest that none of the simple rules based on time and amount can explain the observed differences between the patch and self-control situations. This result challenges the generality of existing models of choice.     

Feeding: Models of Costs and Benefits in Energy Regulation

Models to predict feeding behavior at the level of consumptionand use of energy involve either details of internal (physiological)controls or economic principles of regulation based on optimal(evolutionary) foraging theory. These two approaches will ultimatelybe related, but the former requires more information for specificpredictions. The latter can provide predictions based on selectedcriteria for regulation. Meal sizes and feeding frequencies of hummingbirds are examinedrelative to two regulatory, criteria: maximizing rate of netenergy gain and maximizing efficiency (intakes/expenditures)through a "crop emptying" model that incorporates energy intakefrom food and energy expenditures for short-term (meal to meal)maintenance and longer-term (overnight) energy storage. Experimentalresults suggest that the feeding behavior of hummingbirds isdifferentially sensitive to short-term and daily uses of energy.Changes in overnight energy storage requirements result primarilyin changes in meal size, while changes in meal to meal maintenancerequirements result primarily in feeding frequency changes.The economic models predict these responses. The feeding behaviorof hummingbirds also appears to be sensitive to food quality,time spent flying to and from a food source, and costs associatedwith the weight of ingested food.     

Time and energy constraints and the relationships between currencies in foraging theory

Measured foraging strategies often cluster around values thatmaximize the ratio of energy gained over energy spent whileforaging (efficiency), rather than values that would maximizethe long-term net rate of energy gain (rate). The reasons forthis are not understood. This paper focuses on time and energyconstraints while foraging to illustrate the relationship betweenefficiency and rate-maximizing strategies and develops modelsthat provide a simple framework to analyze foraging strategiesin two distinct foraging contexts. We assume that while capturingand ingesting food for their own use (which we term feeding),foragers behave so as to maximize the total net daily energeticgain. When gathering food for others or for storage (which weterm provisioning), we assume that foragers behave so as tomaximize the total daily delivery, subject to meeting theirown energetic requirements. In feeding contexts, the behaviormaximizing total net daily gain also maximizes efficiency whendaily intake is limited by the assimilation capacity. In contrast,when time available to forage sets the limit to gross intake,the behavior maximizing total net daily gain also maximizesrate. In provisioning contexts, when daily delivery is constrainedby the energy needed to power self-feeding, maximizing efficiencyensures the highest total daily delivery. When time needed torecoup energetic expenditure limits total delivery, a low self-feedingrate relative to the rate of energy expenditure favors efficientstrategies. However, as the rate of self-feeding increases,foraging behavior deviates from efficiency maximization in thedirection predicted by rate maximization. Experimental manipulationsof the rate of self-feeding in provisioning contexts could bea powerful tool to explore the relationship between rate andefficiency-maximizing behavior.     

Deducing implications of fitness maximization when a trade-off exists among alternative currencies

While the theory of natural selection posits that those behaviorsmaximizing reproductive success ("fitness") tend to survive,behavioral ecologists more frequently explain observed behaviorsas maximizing some "currency" on which fitness depends. In thecase of optimal foraging theory, for example, the currency isthe long-term rate of energy intake. This currency approachis adopted because little is known about the form of the fitnessfunction itself. A weakness of the approach is that reproductivesuccess often depends on more than one currency and behaviorswhich augment one currency may reduce another. We explain howto deduce from the hypothesis of fitness maximization testablequalitative and quantitative predictions about behavior whensuch trade-offs exist among currencies and little is known aboutthe fitness function. The methodology we describe is centralto microeconomic theory, and its usefulness explains the centralrole accorded "efficiency conditions" in that theory. We expoundthe approach entirely in terms of two biological examples: apreliminary example involving flower replacement by a perennialand a more elaborate one involving over-winter hoarding by afemale mammal.     

The economic basis of cooperation: tradeoffs between selfishness and generosity

The current study examined the economics of cooperation in controlled-payoffgames by using captive blue jays, Cyanocitta cristata. Thisinvestigation used a special feeding apparatus to test for thestability of cooperative choice in a series of iterated games.The jays experienced experimentally determined game theoreticalpayoff matrices, which determined the distribution of food tothemselves and their opponent, depending on their decision tocooperate or defect. The experiment tested four game matrices,called the cooperate only, defect only, prisoner's dilemma,and opponent control treatments. This study found little cooperationin the defect only and prisoner's dilemma treatments. Cooperationoccurred significantly more often in the opponent control treatment.These findings suggest that the jays attend to short-term consequences;they do not cooperate in the absence of an immediate benefit(defect only), even if a long-term benefit may exist (prisoner'sdilemma). The opponent control treatment suggests that cooperationcan occur when an individual's benefits depend completely onthe actions of others; therefore, generosity is cheap. Thisstudy, therefore, agrees with recent studies in proposing alternativemodels of cooperation.     

Food Intake,Growth and Relatedness in the Subsocial Spider,Stegodyphus lineatus (Eresidae)

One of the presumed benefits of sociality in spiders is an improved foraging success although it has been shown that group feeding is less efficient than feeding alone. In spiders, communal feeding only occurs amongst kin. The effects of relatedness on the consequences of group feeding were investigated in the subsocial spider Stegodyphus lineatus. A significant difference between short-term intake rates and long-term growth rates was shown in a comparison between groups of siblings and groups of non-siblings. Groups of siblings extracted more out of a prey item in a given time and they had higher growth rates than groups of non-siblings.     

The effect of microhabitat feeding site selection on aphid foraging and predation risk

Organisms attempt to optimize foraging by maximizing resource acquisition while minimizing predation risk. Aphids (group-living, phloem-feeding insects) routinely change feeding positions and interact with predators and parasites at the single-leaf scale. Here, we assess the life history and predation risk consequences of within-leaf feeding site choices in pea aphids in response to different natural enemies. First, three-chambered clip cages were used to isolate first instar aphids anterior and posterior to a centrally feeding adult on the underside of a single broad bean leaf. Development time to adulthood did not differ between feeding sites, nor did fecundity within the first 24 h of reproduction. Second, we recorded the frequency and latency of natural enemy attacks on aphids adhered to three leaf sites, matching those of the clip cage experiment, on the underside of a single leaf. Aphids feeding nearest the leaf petiole were at greatest risk of predation by a foliar foraging coccinellid predator, Hippodamia convergens, but not by a parasitoid wasp, Aphidius ervi. Thus, feeding nearer the leaf petiole provided no individual life history benefits and exposes the aphid to increased predation risk. We further discuss the notion that feeding at these sites may provide inclusive fitness benefits for colony mates via alarm signaling and subsequent decreased predation success.     

Simple models of feeding with time and enery contstraints

We analyze how the foraging currencies "rate" (net energy gainper unit time) and "efficiency" (net energy gain per unit energyexpenditure) relate to the workload adopted by a forager. Weconsider feeding (gathering food for immediate consumption)as opposed to provisioning and investigate the influence oftime and energy constraints. In our model the forager may varythe level of energy expenditure while foraging; increased expenditureincreases the rate of gain, but with diminishing returns. Weshow that rate maximizing requires a higher rate of energy expenditurethan efficiency-maximizing, and we compare the performance ofrate- and efficiency-maximizing tactics when the feeding strategyis (1) to maximize the total net gain while foraging; (2) tomaximize the total net daily gain; or (3) to meet a requirement.Generally, the rate-maximizing tactic only performs best whentime is limiting; otherwise, a lighter workload and slower feedingrate perform better. Under the restricted conditions analyzedhere, no general statement can be made about the best tacticwhen the strategy is to meet a requirement. These results mayhelp explain several instances of "submaximal" foraging describedin the literature.     

Carpenter Bee (Xylocopa micans) Risk Indifference and a Review of Nectarivore Risk-sensitivity Studies

This paper presents new results of risk-sensitive foraging studiesof the carpenter bee, Xylocopa micans, and reviews the workto date on risk sensitivity in nectarivores. In the field, nectarivoreschoose among alternative food sources (flowers) that differin the variabilities of their nectar rewards. In the lab, theforaging situation for carpenter bees was experimentally simplifiedby offering the bees a choice between either "low variance"or "high variance" artificial flowers. The two flower typesdiffered in their variabilities but offered the same expectedshortterm rates of net energy gain to test the predictions ofthe short-term rate maximization mechanism. Foragers were testedunder two energy budget conditions, hungry and well-fed, totest the predictions of the z-score model. Individual carpenterbees were indifferent to variability in both nectar volume andnectar sugar concentrations, and their risk-indifference wasunaffected by energy budget. These findings of risk indifferencesupport neither the variance discounting nor the z-score modelof risk sensitivity. Since the low and high variance flowertypes are equivalent for carpenter bees in short-term rate ofenergy gain, there can be no selection on carpenter bees tobe sensitive to variability based on differences in rate ofgain. Studies of risk sensitivity in honey bees and bumble beesusing variance in nectar concentration support this contention.These findings are compared with other nectarivore risk sensitivitystudies in order to highlight the most likely mechanisms underlyingaversion to variation in nectar rewards (short-term rate maximizing,the Weber-Fechner law of perception and learning non-empty flowers)and to suggest future research in the interplay of these threemechanisms.     

Relationships between food resources, foraging patterns, and reproductive success in the water pipit, Anthus sp. spinoletta

A basic but rarely tested assumption in optimal foraging theoryis that positive relationships exist between the foraging patternof an animal, its short-term benefits in feeding, and its long-termfitness. We present evidence for these relationships for a centralplace foraging situation. We studied the foraging behavior ofadult water pipits (Anthus sp. spinoletta) feeding nestlingsin an Alpine habitat near Davos, Switzerland, with the followingresults: (1) searching effort decreases with increasing distancefrom the nest, (2) the amount of prey and the proportion oflarge items brought to the nest increases with increasing foragingdistance, (3) water pipits do not forage according to habitatavailability, but prefer vegetation types with the highest fooddensity (mainly grass and herbs) and avoid those with the lowest,and (4) this selectivity is only expressed when the birds foragemore than 50 m from the nest, i.e., usually outside the territory.Among the several potential interpretations of these results,the most parsimonious is that foraging decisions are based onprofitability, i.e., on the net energy gain per time unit. Additionally,we found that food conditions translate into fitness: the numberof fledglings per nest is related positively to the averageprey biomass at the foraging place and negatively to the averagedistance between the foraging place and the nest. Maximum economicdistances, which were predicted from this food-fitness relationship,agreed well with the actual foraging distances observed. Thissuggests a dose connection between foraging decisions and fitness.In addition to the theoretical issues, some conservation issuesare also briefly discussed.     

Balancing predation risk,social interference,and foraging opportunities in backswimmers,<Emphasis Type="Italic"> Notonecta maculata</Emphasis>

Loss of foraging opportunities and intraspecific competition for prey may be important costs of using refuges, because a hiding animal is unable to use or defend its foraging area from conspecific intrusions. Thus, animals should balance antipredator demands with other requirements in deciding when to come out from a refuge after a predators unsuccessful attack. Observations on foraging and social interactions of backswimmers Notonecta maculata suggest that foraging may be costly in terms of intraspecific agonistic interactions. When prey density is low, increasing the probability of finding a prey may require active exploration of a larger area, but this also increases the probability of encountering a competitor. After simulated exposure to predators, unfed bugs resumed feeding positions after a significantly shorter hiding period than recently fed bugs. We hypothesized that hiding time may also be reduced by recent interactions with conspecific competitors, due to an increased perceived need to defend feeding opportunities. Thus, when a predator attack occurred immediately after an agonistic conspecific interaction, backswimmers resumed feeding positions more quickly, and closer to the original position from which they were disturbed, suggesting short-term defense of particular positions. We conclude that when foraging, backswimmers balance the benefits of finding prey with the costs of predation risk and social interference in deciding their foraging strategy.Communicated by P.K. McGregor     

Sideroxylonal in Eucalyptus foliage influences foraging behaviour of an arboreal folivore

Plant secondary metabolites (PSMs) offer plants chemical defences against herbivores, and are known to influence intake and diet choice in both insect and mammalian herbivores. However, there is limited knowledge regarding how PSMs influence herbivore foraging decisions. Herbivore foraging decisions, in turn, directly impact on which individual plants, and plant species, are selected for consumption. We took advantage of the natural variation in sideroxylonal concentrations in the foliage of Eucalyptus melliodora (Cunn. ex Schauer) to investigate feeding patterns of a marsupial folivore, the common ringtail possum, Pseudocheirus peregrinus (Boddaert 1785). Foliage, collected from six trees, contained between 0.32 and 12.97 mg g-DM^-1 sideroxylonal. With increasing sideroxylonal concentrations, possums decreased their total intake, rate of intake and intake per feeding bout, and increased their cumulative time spent feeding. Possums did not alter their total feeding time, number of feeding bouts or time per feeding bout in response to increasing sideroxylonal concentrations. Results demonstrate important behavioural changes in foraging patterns in response to sideroxylonal. These behavioural changes have important implications, in relation to altered foraging efficiency and potential predation risk, for herbivores foraging in the field. As a result, the spatial distribution of dietary PSMs across a landscape may directly influence herbivore fitness, and ultimately habitat selection of mammalian herbivores.     

Do kleptoparasites reduce their own foraging effort in order to detect kleptoparasitic opportunities?: An empirical test of a key assumption of kleptoparasitic models

Determining if, or when, individuals trade off time spent personally feeding against time spent monitoring others for kleptoparasitism opportunities is essential to an understanding of the evolution of scrounging and usurpation behaviours. We provide a first field test of whether kleptoparasites reduce their personal foraging effort in situations where the frequency and rewards of kleptoparasitism increase. We provided experimental food patches for wild European blackbirds that varied in the distribution of prey and that had a potentially high rate of kleptoparasitism within pairs of blackbirds feeding in them. Although individuals differed in their rate of kleptoparasitism, they did not vary in the size of the reward that they gained from kleptoparasitism. As prey became more clumped, kleptoparasitism rate and its reward per incident increased on average. There was, however, no evidence that individuals that were kleptoparasitising more quickly and/or at a higher frequency had lower personal foraging effort. In contrast, foraging effort increased in both birds compared to when they were foraging alone, independent of dominance, kleptoparasitic opportunity or reward. Our evidence suggests that in some circumstances a kleptoparasite can detect kleptoparasitic opportunities without compromising its own personal foraging rate.     

The strength of selection in the context of migration speed

I use a model of avian migration based on maximization of overall migration speed to compare the strength of selection acting on foraging performance and flight speed. Let the optimal foraging behaviour be u* and the optimal flight speed be v*. It is shown that at this optimum, the ratio of the strength of selection on foraging to the strength of selection on flight speed is theta = -(u*2Pgamma"/v*2gammaP"), where gamma is the rate of energy expenditure during flight and P is the rate at which energy is gained during foraging. The dimensionless ratio P/gamma is the ratio of time spent building up fuel to time spent flying which A. Hedenström and T. Alerstam showed was much greater than unity. Although theta depends on this ratio, it also depends on the curvatures of the functions, as represented by gamma" and P". I use this simple example to make some general points about the strength of selection.     

Begging signals in a mobile feeding system: the evolution of different call types

In some species, dependent offspring join foraging providers and beg for food. Mobile offspring might benefit from evolving begging signals adapted to the different situations they are exposed to, but this possibility has been ignored. In cooperatively breeding meerkats (Suricata suricatta), dependent offspring use a repertoire of several begging calls when joining foraging adults. We found that these calls can be differentiated on the basis of their acoustic structure and that pups adjusted the use of specific call types according to the social context. Pups continuously gave "repeat" calls when they accompanied foraging adults, and playback of these calls increased provisioning by the adults. When pups saw adults with food, they switched from repeat calls to vigorous "high-pitched" calls; adults also preferred to "feed" loudspeakers broadcasting high-pitched calls rather then loudspeakers broadcasting repeat calls. The elaboration of different begging calls might reflect an adaptation to a situation where dependent young must solicit food from potential feeders while at the same time directing feeders to bring the prey item to themselves and not to another begging pup. Here we show that mobile but dependent offspring adapt to different contexts in a mobile feeding system by using a repertoire of begging calls.     

Foraging behaviour of Lesser Sheathbills Chionis minor exploiting invertebrates on a sub-Antarctic island

Summary During winter (May through October) many Lesser Sheathbills Chionis minor at Marion Island in the sub-Antarctic were obliged to leave their preferred foraging habitat in penguin colonies to forage for invertebrates on the island's coastal plain. The study describes factors affecting feeding success, time budgets and predation risk of the sheathbills which exploited these small, patchily dispersed prey. The birds appeared to select prey 1 mm in diameter, and ignore smaller, common invertebrates.Sheathbills were highly selective of foraging habitat. During 17 censuses made through the winter, 97% of the 1,504 birdsightings were at only eight of the 19 available vegetation types. Multiple regression analysis revealed that prey density was the most important criterion in habitat preference, followed by plant canopy height and distance of the habitat from the sea. These variables accounted for 78% of the variance of habitat use. Focal-animal observations in a sample of habitats showed that feeding success was correlated with prey density and distance from the sea. Tall vegetation impeded the locomotion and foraging of sheathbills. The sheathbills reduced predation risk from skuas Catharacta lonnbergi and travelling time by foraging near the shore. The spatial distribution of prey within vegetation types was apparently unimportant in habitat selection.During winter 83% of the sheathbills in the study foraged communally and 98% roosted communally. Flocks occurred only on good quality habitat and flocking probably facilitated habitat selection. Feeding success increased initially with increasing flock size but decreased in flocks greater than 15 birds, which was attributed to localized prey deletions. The sheathbills spent 88% of the daytime foraging; and feeding, looking around and walking comprised 99% of foraging time. Feeding time increased with increasing flock size, looking around decreased but walking was unaffected. Aggression was rare, was unaffected by flock size and did not significantly affect feeding. A probability model showed that sheathbills could greatly reduce predation risk by flocking but the benefits would not improve much in flocks greater than eight birds.The habitat selection, time budgets and feeding success of adults, subadults and juveniles were very similar.The exploitation of terrestrial invertebrates by sheathbills was interpreted as an expansion of the population's trophic niche to tap an underexploited resource on a species-poor island.     

The Behavioral Ecology of Shellfish Gathering in Western Kiribati,Micronesia. 2: Patch Choice,Patch Sampling,and Risk

The prey choice model, previously applied among shellfish gatherers in Kiribati, Micronesia, has shown that they are foraging in a manner that matches the predictions of optimal foraging theory by maximizing their net energy return rates. Similar conclusions can be drawn subsequent to testing the patch choice model, including patch switching; patch sampling; and the analysis of risk. In light of these results, it is argued that natural selection probably never encouraged the persistence of conservation because individuals have nearly always benefited from short-term goals to ensure greater fitness. However, the possibility remains that as a result of changed circumstances brought about by increasing human population, more efficient extractive technologies, and expanding market opportunities, genuine, as opposed to epiphenomenal conservation, may become established in heavily impacted environments.