Testing dynamic variance-sensitive foraging using individual differences in basal metabolic rates of zebra finches

Social foragers can alternate between searching for food (producer tactic), and searching for other individuals that have located food in order to join them (scrounger tactic). Both tactics yield equal rewards on average, but the rewards generated by producer are more variable. A dynamic variance-sensitive foraging model predicts that social foragers should increase their use of scrounger with increasing energy requirements and/or decreased food availability early in the foraging period. We tested whether natural variation in minimum energy requirements (basal metabolic rate or BMR) is associated with differences in the use of producer–scrounger foraging tactics in female zebra finches Taeniopygia guttata . As predicted by the dynamic variance-sensitive model, high BMR individuals had significantly greater use of the scrounger tactic compared with low BMR individuals. However, we observed no effect of food availability on tactic use, indicating that female zebra finches were not variance-sensitive foragers under our experimental conditions. This study is the first to report that variation in BMR within a species is associated with differences in foraging behaviour. BMR-related differences in scrounger tactic use are consistent with phenotype-dependent tactic use decisions. We suggest that BMR is correlated with another phenotypic trait which itself influences tactic use decisions.     

Producer–Scrounger Games in a Spatially Explicit World: Tactic Use Influences Flock Geometry of Spice Finches

Group-foraging animals can either search for their food (producer) or search for opportunities to join the food discoveries of others (scrounger). To maximize food returns, producers should distance themselves from potential competitors whereas scroungers should increase proximity to potential producers. We investigated the extent to which playing one or the other tactic affected an individual's location in captive flocks of ground-feeding spice finches ( Lonchura punctulata ) as they foraged for hidden clumps of food on an aviary floor. We constrained some individuals to use the producer tactic by pre-training them to find food hidden under lids. Constrained producers foraged significantly further from the center of flocks than constrained scroungers. Flocks with many scroungers were significantly more compact than flocks with fewer scroungers. The results are consistent with published simulations of spatially explicit producer–scrounger models and suggest that the use of producer and scrounger foraging tactics be included as a factor that affects an individual's position within foraging groups.     

Phenotypic Correlates of Scrounging Behavior in Zebra Finches: Role of Foraging Efficiency and Dominance

In flocks, individuals can search for their own food using the producer tactic or exploit the discoveries of companions using the scrounger tactic. Models of the producer–scrounger game usually assume that tactic payoffs are independent of individual phenotypic traits. However, factors such as dominance status or foraging efficiency may constrain the use of tactics and lead to asymmetric tactic use among individuals. For instance, in flocks composed of foragers with unequal foraging efficiency, foragers that are less efficient at obtaining food are expected to rely on the scrounger tactic to a greater extent. I examined the role of foraging efficiency and dominance status as potential correlates of scrounging behavior in small aviary flocks of zebra finches (Taenopygia guttata). Individual foraging efficiency was documented in each flock in a treatment that prevented scrounging. In a subsequent treatment that allowed scrounging, higher levels of scrounging occurred as predicted in foragers with lower foraging efficiency. Dominance status was a poor predictor of tactic choice. Birds that arrived later on the foraging grid foraged less efficiently when scrounging was prevented and used scrounging to a greater extent when allowed, suggesting a link between boldness, foraging efficiency and the choice of foraging tactics in small flocks of zebra finches.     

Incompatibility between antipredatory vigilance and scrounger tactic in nutmeg mannikins, Lonchura punctulata

Most social foragers must search for food while avoiding predators. Group-foraging nutmeg mannikins engaged in a producer-scrounger game search for their own food (play producer) by hopping with the head down and search for others' food discoveries (play scrounger) by hopping with the head up. If the scrounger tactic is compatible with antipredatory vigilance, then an increase in antipredatory vigilance should lead to the detection of more joining opportunities, and hence to more joining by foragers. We tested this prediction as well as the extent to which stationary birds use head up exclusively for antipredatory purposes and hopping birds use head up for foraging purposes only. We observed three flocks of nutmeg mannikins searching for hidden clumps of food in an indoor aviary. We used a 2×2 factorial design in which both the distance to a safe refuge and the food distribution were manipulated. The use of head up by stationary and eating birds increased significantly with increased distance to cover. Distance to cover, however, had no effect on the use of the scrounger tactic or on the level of joining. We found no evidence of compatibility between the scrounger tactic and antipredatory vigilance. Our results provide the first unambiguous evidence for the existence of two distinct and incompatible patterns of vigilance for predators and for conspecifics. Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.      

The Effect of Within-Flock Spatial Position on the Use of Social Foraging Tactics in Free-Living Tree Sparrows

The benefit of producer (searches for own food) or scrounger (exploits the others’ food discoveries) foraging tactic in a group of socially feeding animals may depend on where the individual searches for food within the group. Scrounging may be more advantageous in the centre of the group, having more individuals around to join, while producing may be more beneficial at the edges, where more unexplored food patches may be found. This study shows within‐flock position correlates with foraging tactic use of feeding birds in socially foraging tree sparrows, Passer montanus. Sparrows staying closer to the centre of the flock found their food patches more frequently by joining (i.e. use more frequently the scrounging tactic) than those staying toward the edges. To our knowledge this is the first field study demonstrating the relationship between spatial position and foraging tactic use. We investigated this relationship under different perceived predation hazard, and found that under elevated risk of predation, central individuals may increase their use of joining more than individuals on the periphery of the flock. Moreover, we show that extremely specialized use of searching tactics may be very infrequent in tree sparrows. As both within‐flock position and search tactic use can be altered very quickly and without leaving the flock, individuals may easily alter them in order to adjust their behaviour.     

Experimental evidence that group foragers can converge on predicted producer-scrounger equilibria

When foraging together, animals are often observed to feed from food discoveries of others. The producer-scrounger (PS) game predicts how frequently this phenomenon of food parasitism should occur. The game assumes: (1) at any moment all individuals can unambiguously be categorized as either playing producer (searching for undiscovered food resources) or scrounger (searching for exploitation opportunities), and (2) the payoffs received from the scrounger tactic are negatively frequency dependent; a scrounger does better than a producer when the scrounger tactic is rare, but worse when it is common. No study to date has shown that the payoffs of producer and scrounger conform to the game's assumptions or that groups of foragers reach the predicted stable equilibrium frequency (SEF) of scrounger, whereby both tactics obtain the same payoff. The current study of three captive flocks of spice finches, Lonchura punctulata, provides the first test of the PS game using an apparatus in which both assumptions of the PS game are met. The payoffs to the scrounger, measured as feeding rate (seeds/s), were highly negatively frequency dependent on the frequency of scrounger. The feeding rate for scrounger declined linearly while the rate for producer either declined only slightly or not at all with increasing scrounger frequency. When given the opportunity to alternate between tactics, the birds changed their use of each, such that the group converged on the predicted SEF of scrounger after 5-8 days of testing. Individuals in this study, therefore, demonstrated sufficient plasticity in tactic use such that the flock foraged at the SEF of scrounger. Copyright 2000 The Association for the Study of Animal Behaviour.     

The effects of predation risk on the use of social foraging tactics

The effects of predation on the use of social foraging tactics, such as producing and scrounging, are poorly known in animals. On the one hand, recent theoretical models predict increased use of scrounging with increasing predation risk, when scroungers seeking feeding opportunities also have a higher chance of detecting predators. On the other hand, there may be no relation between tactic use and predation when antipredator vigilance is not compatible with scanning flockmates. We investigated experimentally the effects of predation risk on social foraging tactic use in tree sparrows, Passer montanus. We manipulated predation risk in the field by changing the distance between shelter and a feeder. Birds visited the feeder in smaller flocks, spent less time on it and were somewhat more vigilant far from shelter than close to it. Increased predation risk strongly affected the social foraging tactic used: birds used the scrounger tactic 30% more often far from cover than close to it. Between-flock variability in scrounging frequency was not related to the average vigilance level of the flock members, and within-flock variability in the use of scrounging was negatively related to the vigilance of birds. Our results suggest that in tree sparrows, the increased frequency of scrounging during high predation risk cannot simply be explained by an additional advantage of increasing antipredator vigilance. We propose alternative mechanisms (e.g. increased stochasticity in food supply, and that riskier places are used by individuals with lower reserves) that may explain increased scrounging when animals forage under high predation risk.     

Risky decisions: a test of risk sensitivity in socially foraging flocks of Lonchura punctulata

Group foraging allows for individuals to exploit the food discoveriesof other group members. If searching for food and searchingfor exploitation opportunities within a group are mutually exclusivealternatives, the decision to use one or the other is modeledas a producer-scrounger game because the value of each alternativeis frequency dependent. Stochastic producer-scrounger modelsgenerally assume that producer provides a more variable anduncertain reward than does the scrounger and hence is a riskierforaging alternative. Socially foraging animals that are attemptingto reduce their risk of starvation should therefore alter theiruse of producer and scrounger alternatives in response to changesin energy budget. We observed flocks of nutmeg mannikins (L.punctulata) foraging in an indoor aviary to determine whethertheir use of producer and scrounger alternatives were risk sensitive.Analyses of the foraging rewards of three flocks of seven birdsconfirm that producer is a riskier foraging strategy than isscrounger, although the difference in risk is rather small.We then submitted two other flocks to two different energy budgetsand observed the foraging decision of four focal birds in eachflock. All but one bird increased their relative use of theriskier producer strategy in the low food reserve treatment,but the overall use of producer did not differ significantlybetween treatments, providing evidence for a small but consistenteffect.     

Learning in a game context: strategy choice by some keeps learning from evolving in others

Behavioural decisions in a social context commonly have frequency-dependent outcomes and so require analysis using evolutionary game theory. Learning provides a mechanism for tracking changing conditions and it has frequently been predicted to supplant fixed behaviour in shifting environments; yet few studies have examined the evolution of learning specifically in a game-theoretic context. We present a model that examines the evolution of learning in a frequency-dependent context created by a producer–scrounger game, where producers search for their own resources and scroungers usurp the discoveries of producers. We ask whether a learning mutant that can optimize its use of producer and scrounger to local conditions can invade a population of non-learning individuals that play producer and scrounger with fixed probabilities. We find that learning provides an initial advantage but never evolves to fixation. Once a stable equilibrium is attained, the population is always made up of a majority of fixed players and a minority of learning individuals. This result is robust to variation in the initial proportion of fixed individuals, the rate of within- and between-generation environmental change, and population size. Such learning polymorphisms will manifest themselves in a wide range of contexts, providing an important element leading to behavioural syndromes.     

Daily Patterns of Optimal Producer and Scrounger Use under Predation Hazard: A State-Dependent Dynamic Game Analysis

Feeding in groups often gives rise to joining: feeding from other's discoveries. The joining decision has been modeled as a producer-scrounger game where the producer strategy consists of searching for one's food and the scrounger strategy consists of searching for food discovered by others. Previous models revealed that the evolutionarily stable proportion of scrounging mostly depends on the fraction of each food patch available only to its producer. These early models are static and state independent and are therefore unable to explore whether the time of day, the animal's state, and the degree of predation hazard influence an individual's decision of whether to use the producer or scrounger strategy. To investigate these issues, we developed a state-dependent dynamic producer-scrounger game model. The model predicts that, early in the day, low reserves promote a preference for the scrounger strategy, while the same condition late in the day favors the use of the producer strategy. Under rich and clumped food, the availability of scrounging can improve the daily survival of any average group member. The model suggests only weak effects of predation hazard on the use of scrounging. Future developments should consider the effects of dominance asymmetries and allowing foragers a choice between foraging alone or in a group harboring an evolutionarily stable frequency of scrounger.     

Overriding the oddity effect in mixed-species aggregations: group choice by armored and nonarmored prey

Because "odd" individuals often suffer disproportionately highrates of predation, solitary individuals should join groupswhose members are most similar to themselves in appearance.We examined group-choice decisions by individuals in armoredand nonarmored species and predicted that either (1) the oddityeffect would result in preference for conspecific groups forsolitary individuals of both species, or (2) individuals inthe armored species would prefer to associate with groups containingindividuals of the more vulnerable species. Armored brook sticklebacks(Culaea inconstans) and nonarmored fathead minnows (Pimephalespromelas) have the same predators and often occur together instreams. In mixed-species shoals, yellow perch (Perca flavescens)attacked minnows earlier and more often than sticklebacks. Wetested whether solitary minnows and sticklebacks preferred toassociate with conspecific or heterospecific shoals under conditionsof both low and high predation risk. When predation risk washigh, minnows preferred to associate with conspecifics overheterospecifics, as predicted by the oddity effect. In contrast,sticklebacks preferentially associated with groups of minnowsover groups of conspecifics when predation risk was high. Whenpredation risk was low, solitary individuals of both speciespreferentially associated with conspecific over heterospecificshoals. Stickleback shoal choices under low-risk conditionsmay have been influenced by interspecific competition for food.In feeding experiments, minnows were more efficient foragersthan sticklebacks, so it should benefit sticklebacks to avoidminnows unless predation risk is high. Therefore, for armoredprey, the benefits of associating with more vulnerable preyappear to override the costs of both the oddity effect and foodcompetition when predation risk is high.     

Geometry for a selfish foraging group: a genetic algorithm approach

The advantages of group living are not shared equally among all group members and these advantages may depend on the spatial position occupied by a forager within the group. For instance, it is thought that socially dominant individuals prefer the predator-safe central position of groups forcing subordinates to the periphery. Uneven spread of benefits among group members can occur when some animals (the scroungers) parasitically exploit the food findings of other foragers (the producers). Here we focus on how playing producer or scrounger affects an individual''s spatial position within a group. We model the movement of foraging animals playing scrounger or producer using a spatially explicit simulation and use a genetic algorithm to establish movement rules. We find that groups containing producers and scroungers are more compact compared to an equivalent group of producers only. Furthermore, the position occupied by strategies varies: scroungers are mainly found in central positions, while producers in the periphery, suggesting that the best position for strategies differs. Dominants, therefore, should prefer movement rules which lead to central positions because of the positional benefits provided to the scrounger strategy they use. Moreover, position within a group will introduce an asymmetry among otherwise phenotypically symmetric individuals.     

Predator inadvertent social information use favours reduced clumping of its prey

When animals forage socially, individuals can obtain prey from their own searching (producer tactic) or by using the behaviour of others (scrounger tactic) when it provides inadvertent social information (ISI) that food has been located. This ISI may either indicate the location of food (social information, SI), or it may indicate the quality of the resource (public information, PI). To date, few studies have explored the selective consequences for prey of being exploited by predators that use ISI. Prey exploited by such predators should evolve traits that favour high levels of ISI use (scrounging) because this would result in lower predator search efficiency given that fewer predators would be searching directly for the prey. Our simulations confirm that ISI‐using predators should increase their use of ISI when their prey form larger clumps resulting in higher prey survival. Our objective therefore is to explore whether prey will evolve towards higher clumpiness when their predators use ISI, using genetic algorithm simulation. The prey were subjected to one of three types of predators for over 500 prey generations. The predators either used: (1) no social information (NS), (2) SI only, or (3) PI. Surprisingly, the prey evolved the highest clumpiness for NS predators. Prey evolved towards smaller clump sizes with SI predators and the clumps were marginally larger when predators used PI. The result is due to the prey evolving the minimum clumpiness required to cause maximal ISI use by their predators. We discuss how this response by prey may favour the use of PI over SI in their ISI‐using predators.     

Distress calls reflect poxvirus infection in lesser short-toed lark Calandrella rufescens

Several studies have highlighted the association between birdsong and parasite load, but there is no evidence regarding therelationships among pathogens and alarm or distress calls, whichare used in antipredator strategies. We analyzed the associationbetween virus infection and the distress calls of lesser short-toedlark (Calandrella rufescens), addressing the relationships betweencall acoustic properties, presence of poxvirus lesions, andother measurements of bird health (body condition, T-cell–mediatedimmune response, heterophils-to-lymphocytes ratio [H/L ratio],and blood parasites). The study was carried out in Fuerteventura(Canary Islands), where 55% of lesser short-toed larks wereinfected. Pox infection was associated with changes in the spectrotemporalstructure of lark distress calls and affected the condition-dependentnature of these signals. Virus bearers uttered significantlyshorter and lower pitched calls than virus-free birds, givingeven shorter calls when subject to greater physiological stress(higher H/L ratio), whereas virus-free individuals did the opposite.Call harshness was positively correlated with bird immune andbody condition, independently of virus infection, whereas callpulse rate decreased in stressed birds. We hypothesize thathealthy birds might reveal their ability to bear the costs ofantipredator defense by means of long, harsh, and fast modulateddistress calls. Infection not only affects individual stateand morphology by means of gross lesions but also may altera signal used in an antipredator context, thus potentially reducingbird fitness both directly (through disease) and indirectly(through increased predation).     

The effect of prior residence and pair bond on scrounging choices in flocks of zebra finches, Taenopygia guttata

In groups, animals can use the producer tactic to locate food patches and the scrounger tactic to join the food discoveries of other companions. At equilibrium, models predict a mixture of the two tactics with equal payoffs. Several factors may constrain the use of tactics and lead to biases in scrounging choices. I explored the effect of prior residence and pair bond as potential constraints on scrounging choices in flocks of zebra finches (Taenopygia guttata). Experimental flocks contained two birds already established in an aviary (prior residents) and two birds recently released in the aviary for the first time (new residents). All birds were previously trained to find food on a foraging grid. In the aviary, new residents followed prior residents from perches to the grid and relied heavily on prior residents to locate food patches. Low initial success by new residents probably favoured heavy reliance on the scrounger tactic. New residents that formed pair bonds with prior residents foraged closer to their mates and scrounged selectively from their mates in some cases. Prior residence, and pair bond to a lesser extent, influenced scrounging choices in zebra finches and could lead to deviation from the expected use of foraging tactics.     

Antipredator Benefits of Schooling Behaviour in a Cyprinodontid Fish,the Banded Killifish (Fundulus diaphanus)

Fish schools are believed to provide antipredator benefits to their members. Two potential antipredator benefits, the dilution and confusion effects, of schooling were investigated in the laboratory using banded killifish (Fundulus diaphanus). Individual risk of being attacked and killed by a fish predator (white perch, Morone americana) declined with increasing killifish school size in a manner closely predicted by the dilution hypothesis. Perch were apparently not confused by schooling killifish since fish in groups of one did not suffer a disproportionately greater predation rate than fish in all larger school sizes. However, killifish straggling from the school were preferentially attacked and more successfully captured compared with school members. Schooling in the banded killifish therefore confers a considerable antipredator benefit to individual group members, at least through a dilution effect, and straying from a school has an associated increased risk of mortality to predation, which selects for schooling behaviour.     

Increased performance of offspring sired by parasitic males in bluegill sunfish

Males of many species are characterized by alternative matingtactics. In bluegill sunfish (Lepomis macrochirus), some malesdelay maturation and become "parentals" while other males matureprecociously and become "cuckolders." Parentals use an overt,territorial mating tactic, defending a nest and courting females.Cuckolders instead use a sneaking tactic to parasitize parentals.It has previously been shown that parentals that are heavilycuckolded provide less care to their young, yet females do notappear to discriminate against cuckolders, and they may actuallyrelease more eggs when a cuckolder is present than when spawningonly with a parental. Here I examined growth rate of fry ofknown paternity through the yolk-sac stage of development usingcomplementary laboratory and field studies to assess a potentialindirect benefit for females that mate with cuckolders. Comparisonof maternal half-siblings sired in vitro shows that cuckolderoffspring grow faster and to a larger size than parental offspringwhile feeding endogenously on their yolk sac. Because both foodresource and maternal genes are equivalent across treatments,these data indicate a genetic difference in growth between thetwo male life histories. In the field, fry from nests that haveproportionately more cuckolder offspring are larger when theyemerge from the nest. This increased size can lead to threefoldhigher survivorship for cuckolder offspring than parental offspringfrom Hydra canadensis predation, a major predator of bluegillfry. These results are discussed in the context of mate choicefor direct and indirect benefits and in the context of the evolutionof alternative mating tactics.     

Behavior and temperature modulate a thermoregulation–predation risk trade‐off in juvenile gopher tortoises

Ectotherms frequently thermoregulate behaviorally to improve physiological processes such as digestion and growth, but basking and other thermoregulatory activities can also increase predation risk. Organismal and environmental characteristics can, in some species, influence predation risk associated with thermoregulation and thereby relax or tighten constraints on thermoregulatory behavior, physiological performance, and, ultimately, life history traits. Providing one of the first such investigations in turtles, we examine whether behavior and thermal environment modulate a thermoregulation–predation risk trade‐off in juvenile gopher tortoises (Gopherus polyphemus). Young gopher tortoises experience very high predation pressure, and their declining species faces many challenges, including human‐induced increased shading of its environment. We hypothesized that in response to simulated predator approach, basking hatchling and juvenile tortoises would: (i) hide inside burrows; (ii) hide for shorter durations in cooler burrows presumably due to greater constraints on physiological performance; and (iii) spend greater time at the surface following disturbance in cool environments because individuals would need to bask more to maintain preferred body temperatures. Basking tortoises always hid inside burrows when approached and exhibited very long flight initiation distances ( = 45 m) that increased with age/size. Individuals fled into burrows even when it was not possible for them to see the approaching researcher, suggesting the use of vibrations (aerial/ground) to detect potential predators and a possible antipredator function for exceptionally large otoliths characteristic of the species. Tortoises hid for short durations ( = 18.3 min), especially in cool burrows, suggesting that they optimize hiding responses to balance physiological costs and antipredator benefits. Additionally, surface activity following disturbance consisted primarily of basking and correlated negatively with burrow temperature. These findings suggest that thermal environment influences predation risk in ectotherms whose surface activity is driven primarily by thermoregulatory requirements and highlight potential benefits of warm, well‐insolated habitats, such as endangered longleaf pine (Pinus palustris) ecosystems, for juvenile gopher tortoises.     

Learning temporal patterns of risk in a predator-diverse environment

Predation plays a major role in shaping prey behaviour. Temporal patterns of predation risk have been shown to drive daily activity and foraging patterns in prey. Yet the ability to respond to temporal patterns of predation risk in environments inhabited by highly diverse predator communities, such as rainforests and coral reefs, has received surprisingly little attention. In this study, we investigated whether juvenile marine fish, Pomacentrus moluccensis (lemon damselfish), have the ability to learn to adjust the intensity of their antipredator response to match the daily temporal patterns of predation risk they experience. Groups of lemon damselfish were exposed to one of two predictable temporal risk patterns for six days. "Morning risk" treatment prey were exposed to the odour of Cephalopholis cyanostigma (rockcod) paired with conspecific chemical alarm cues (simulating a rockcod present and feeding) during the morning, and rockcod odour only in the evening (simulating a rockcod present but not feeding). "Evening risk" treatment prey had the two stimuli presented to them in the opposite order. When tested individually for their response to rockcod odour alone, lemon damselfish from the morning risk treatment responded with a greater antipredator response intensity in the morning than in the evening. In contrast, those lemon damselfish previously exposed to the evening risk treatment subsequently responded with a greater antipredator response when tested in the evening. The results of this experiment demonstrate that P. moluccensis have the ability to learn temporal patterns of predation risk and can adjust their foraging patterns to match the threat posed by predators at a given time of day. Our results provide the first experimental demonstration of a mechanism by which prey in a complex, multi-predator environment can learn and respond to daily patterns of predation risk.     

Squeezing out the last egg—annual fish increase reproductive efforts in response to a predation threat

Both constitutive and inducible antipredator strategies are ubiquitous in nature and serve to maximize fitness under a predation threat. Inducible strategies may be favored over constitutive defenses depending on their relative cost and benefit and temporal variability in predator presence. In African temporary ponds, annual killifish of the genus Nothobranchius are variably exposed to predators, depending on whether larger fish invade their habitat from nearby rivers during floods. Nonetheless, potential plastic responses to predation risk are poorly known. Here, we studied whether Nothobranchius furzeri individuals adjust their life history in response to a predation threat. For this, we monitored key life history traits in response to cues that signal the presence of predatory pumpkinseed sunfish (Lepomis gibbosus). While growth rate, adult body size, age at maturation, and initial fecundity were not affected, peak and total fecundity were higher in the predation risk treatment. This contrasts with known life history strategies of killifish from permanent waters, which tend to reduce reproduction in the presence of predators. Although our results show that N. furzeri individuals are able to detect predators and respond to their presence by modulating their reproductive output, these responses only become evident after a few clutches have been deposited. Overall our findings suggest that, in the presence of a predation risk, it can be beneficial to increase the production of life stages that can persist until the predation risk has faded.