Producing and scrounging can have stabilizing effects at multiple levels of organization

This study shows, for the first time, that the evolution of a simple behavior, scrounging, at the individual level can have effects on populations, food chains, and community structure. In particular, the addition of scrounging in consumer populations can allow multiple consumers to coexist while exploiting a single prey. Also, scrounging in the top predator of a tritrophic food chain can stabilize interactions between the top predator, its prey, and its prey's prey. This occurs because the payoffs to scrounging for food in a population are negative frequency dependent, allowing scroungers to invade a population and to coexist with producers at a frequency which is density‐dependent. The presence of scroungers, who do not search for resources but simply use those found by others (producers) reduces the total amount of resource acquired by the group. As scrounging increases with group size, this leads to less resource acquired per individual as the group grows. Ultimately, this limits the size of the group, its impact on its prey, and its ability to outcompete other species. These effects can promote stability and thus increase species diversity. I will further suggest that prey may alter their spatial distribution such that scrounging will be profitable among their predators thus reducing predation rate on the prey.     

Patch exploitation in a producer-scrounger system: test of a hypothesis using flocks of spice finches (Lonchura punctulata)

Group foraging allows individuals (scroungers) to obtain fooddiscovered by others (producers). Producer-scrounger game modelstypically overlook the costs and benefits of patch exploitation,assuming instead that producers and scroungers abandon patchessimultaneously once depletion occurs. Here we develop an extensionof the marginal value theorem of patch exploitation that includesthe producer-scrounger dynamics and examine the propensity ofa producer to abandon its patch before depletion once scroungersarrive. We predict that early departures should occur more oftenwhen expected searching time decreases and when competitionintensity in the patch increases. Competition intensity is expectedto increase when more scroungers are present or when patchesare smaller. We tested these predictions using a within-subjectexperimental design with six captive flocks of spice finches(Lonchura punctulata), each composed of one producer and threescroungers. As predicted, producers abandoned their food discoveriesmore frequently once scroungers arrived when searching timewas short, when more scroungers were present, and when patcheswere small. The results show that the producers of a patch oftenleave as scroungers join their food discoveries because thepayoffs from leaving exceed those from staying     

Scrounging Tactics in Free-Ranging Ravens, Corvus corax

Social foraging allows individuals to scrounge, i.e. to exploit the food others have made available. The conditions promoting scrounging as an alternative foraging tactic have yet received limited attention. We presently examine whether ravens, as opportunistic scavengers, adjust their foraging tactics according to the potential costs involved in accessing a particular food source. We observed wild ravens foraging in a game park, at the enclosures of wolves, Canis lupus, and wild boars, Sus scrofa. Wolves may aggressively defend their food and even kill ravens, whereas wild boars do not. When co‐feeding with wolves, the ravens showed higher scrounging rates than with wild boars. Only at the wolves, they tended to specialize either on scrounging or on getting food directly from the site. However, scrounging techniques differed in relation to the state of food depletion. Early on, after food became available, the ravens most frequently displaced others from food, whereas towards the end, stealing, solicited sharing, and cache raiding became prevalent. These techniques differed in their profitability and their use was related to the scroungers’ age, social status and affiliative relationships. This suggests that ecological conditions, such as co‐feeding with potential predators, may influence the individuals’ decision whether or not to scrounge in competition for food. Social conditions, on the other hand, may affect the way how to get at food possessed by others and may thus, to a large extent, determine the profitability of scrounging.     

Scrounging behavior regulates population dynamics

The integration of behavioral and population ecology is necessary when behavior both feeds into demographic parameters and depends on population parameters. We show that scrounging behavior, the exploitation of others' resources, can affect both demographic parameters and population dynamics, including the stability of interactions with prey. Scrounging is a common tactic and its pay-offs exhibit both density- and frequency-dependence. We demonstrate that scrounging can act as a population regulator through its effects on individuals' reproductive rate and mortality. We also explore its effects on predator-prey population dynamics and show that the presence of scrounging predators allows an increased predator population size and contributes to the regulation of both predator and prey populations. Behavioral ecologists will appreciate that although scrounging is often pictured as imposing a social foraging cost to group membership, at the population level it also allows higher numbers of both prey and predators to coexist at equilibrium.     

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.     

Advantages of social foraging in crab spiders: Groups capture more and larger prey despite the absence of a web

Among group‐living spiders, subsocial representatives in the family of crab spiders (Thomisidae) are a special case, as they build protective communal leaf nests instead of extensive communal capture webs. It could thus be inferred that antipredator benefits (e.g., enhanced protection in larger nests) rather than foraging‐related advantages (e.g., capture of more and larger prey) promote sociality in this family. Nonetheless, subsocial crab spiders do share prey, and if this behaviour does not reflect mere food scramble but has a cooperative character, crab spiders may offer insights into the evolution of social foraging applicable to many other cooperative predators that hunt without traps. Here, we performed a comparative laboratory feeding experiment on three of the four subsocial crab spider species—Australomisidia ergandros, Australomisidia socialis and Xysticus bimaculatus—to determine if crab spiders derive advantages from foraging in groups. In particular, we tested artificially composed groups of five sibling spiderlings vs. single siblings in terms of prey capture success and prey size preference. Across species, groups had higher prey capture success (measured in terms of capture rates and capture latency) and were more likely to attack large, sharable prey—dynamics leading to reduced food competition among group members in favour of living and foraging in groups. Within groups, we further compared prey extraction efficiency among the three applied social foraging tactics: producing, scrounging and feeding alone. In A. ergandros, individuals were exceptionally efficient when using the non‐cooperative scrounger tactic, which entails feeding on the prey provided by others. Thus, our multispecies comparison confirms foraging advantages in maintaining a cooperative lifestyle for crab spiders, but also demonstrates the relevance of research into exploitation of cooperative foraging in this family.     

Consequences of multiple simultaneous opportunities to exploit others’ efforts on free riding

Individuals within a group do not all act in the same way: Typically, the investors (or producers) put efforts into producing resources while the free riders (or scroungers) benefit from these resources without contributing. In behavioral ecology, the prevalence of free riders can be predicted by a well‐known game‐theoretical model—the producer–scrounger (PS) model—where group members have the options to either search for resources (producers) or exploit the efforts of others (scroungers). The PS model has received some empirical support, but its predictions, surprisingly, are based on the strict assumption that only one resource can be exploited at a time. Yet, multiple simultaneous opportunities to exploit others’ efforts should frequently occur in nature. Here, we combine analytic and simulation approaches to explore the effect of multiple simultaneous scrounging opportunities on tactic use. Our analyses demonstrate that scrounging rates should increase with the number of simultaneous opportunities. As such, the amount and spatial distribution (i.e., clumped vs. dispersed) of resources as well as the risk of predation are key predictors of scrounging behavior. Because scroungers contribute to reducing the speed of resource exploitation, the model proposed here has direct relevance to the exploitation and sustainability of renewable resources.     

Wild Carib grackles play a producer scrounger game

Producer–scrounger (PS) game-theoretical foraging modelsmake predictions about the decision of group-feeding animalseither to look for food (produce) or for opportunities to exploitthe discoveries of other foragers (scrounge). We report themost complete demonstration to date of the applicability ofthe PS foraging game in a free-living animal, the Carib grackle(Quiscalus lugubris) of Barbados. As assumed by PS games, thepayoffs obtained by scroungers were negatively frequency dependent.Experimentally, increasing the cost of scrounging led to a decreasein the observed proportion of scroungers, whereas raising thecost of producing increased the proportion of scroungers. Observationsof marked birds revealed that group-level changes could be broughtabout by individual flexibility in tactic use. Despite consistentindividual differences in tactic use, most birds used both tacticsand could alter their use of producing and scrounging when conditionschanged. We found no difference in the payoffs obtained by producersand scroungers, suggesting a symmetrical game equilibrium. Ourresults call for testing the PS foraging game in a broader rangeof biological systems that include different types of scroungingbehavior (e.g., scramble, stealthful, or aggressive scrounging)as well as the exploitation of different phases of food production(e.g., searching, handling).     

The patch distributed producer-scrounger game

Grouping in animals is ubiquitous and thought to provide group members antipredatory advantages and foraging efficiency. However, parasitic foraging strategy often emerges in a group. The optimal parasitic policy has given rise to the producer-scrounger (PS) game model, in which producers search for food patches, and scroungers parasitize the discovered patches. The N-persons PS game model constructed by Vickery et al. (1991. Producers, scroungers, and group foraging. American Naturalist 137, 847-863) predicts the evolutionarily stable strategy (ESS) of frequency of producers that depends on the advantage of producers and the number of foragers in a group. However, the model assumes that the number of discovered patches in one time unit never exceeds one. In reality, multiple patches could be found in one time unit. In the present study, we relax this assumption and assumed that the number of discovered patches depends on the producers’ variable encounter rate with patches (λ). We show that strongly depends on λ within a feasible range, although it still depends on the advantage of producer and the number of foragers in a group. The basic idea of PS game is the same as the information sharing (parasitism), because scroungers are also thought to parasitize informations of locations of food patches. Horn (1968) indicated the role of information-parasitism in animal aggregation (Horn, H.S., 1968. The adaptive significance of colonial nesting in the Brewer's blackbird (euphagus cyanocephalus). Ecology 49, 682-646). Our modified PS game model shows the same prediction as the Horn's graphical animal aggregation model; the proportion of scroungers will increase or animals should adopt colonial foraging when resource is spatiotemporally clumped, but scroungers will decrease or animals should adopt territorial foraging if the resource is evenly distributed.     

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.     

Foraging mode affects the evolution of egg size in generalist predators embedded in complex food webs

Ecological networks incorporate myriad biotic interactions that determine the selection pressures experienced by the embedded populations. We argue that within food webs, the negative scaling of abundance with body mass and foraging theory predict that the selective advantages of larger egg size should be smaller for sit‐and‐wait than active‐hunting generalist predators, leading to the evolution of a difference in egg size between them. Because body mass usually scales negatively with predator abundance and constrains predation rate, slightly increasing egg mass should simultaneously allow offspring to feed on more prey and escape from more predators. However, the benefits of larger offspring would be relatively smaller for sit‐and‐wait predators because (i) due to their lower mobility, encounters with other predators are less common, and (ii) they usually employ a set of alternative hunting strategies that help to subdue relatively larger prey. On the other hand, for active predators, which need to confront prey as they find them, body‐size differences may be more important in subduing prey. This difference in benefits should lead to the evolution of larger egg sizes in active‐hunting relative to sit‐and‐wait predators. This prediction was confirmed by a phylogenetically controlled analysis of 268 spider species, supporting the view that the structure of ecological networks may serve to predict relevant selective pressures acting on key life history traits.     

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.     

Diseased Social Predators

Social predators benefit from cooperation in the form of increased hunting success, but may be at higher risk of disease infection due to living in groups. Here, we use mathematical modeling to investigate the impact of disease transmission on the population dynamics benefits provided by group hunting. We consider a predator–prey model with foraging facilitation that can induce strong Allee effects in the predators. We extend this model by an infectious disease spreading horizontally and vertically in the predator population. The model is a system of three nonlinear differential equations. We analyze the equilibrium points and their stability as well as one- and two-parameter bifurcations. Our results show that weakly cooperating predators go unconditionally extinct for highly transmissible diseases. By contrast, if cooperation is strong enough, the social behavior mediates conditional predator persistence. The system is bistable, such that small predator populations are driven extinct by the disease or a lack of prey, and large predator populations survive because of their cooperation even though they would be doomed to extinction in the absence of group hunting. We identify a critical cooperation level that is needed to avoid the possibility of unconditional predator extinction. We also investigate how transmissibility and cooperation affect the stability of predator–prey dynamics. The introduction of parasites may be fatal for small populations of social predators that decline for other reasons. For invasive predators that cooperate strongly, biocontrol by releasing parasites alone may not be sufficient.     

The Payoffs to Producing and Scrounging: What Happens when Patches are Divisible?

Although many group-foraging models assume that all individuals search for and share their food equally, most documented instances of group foraging exhibit specialized use of producer and scrounger strategies. In addition, many of the studies have focused on groups with strong individual asymmetries exploiting food that is not easily divisible. In the present study we describe individual foraging behavior of relatively nonaggressive flock foragers exploiting divisible clumps of food. Two experiments, one with flocks of spice finches and another with flocks of zebra finches, suggest that divisibility of food patches may have important consequences for social foraging behavior. Neither dominance nor the distribution and quality of food patches affect the relative advantage that producing individuals enjoy over those that scrounge. Specialized producers and scroungers are absent from flocks of both species. Systems where patches are shared may differ fundamentally from those where patches are monopolized by scroungers.     

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.     

Producers and scroungers: A general model and its application to captive flocks of house sparrows

Many forms of interaction within and between species appear to be based on ‘scrounger’ individuals or species exploiting a limited resource provided ‘producers’. A mathematical model is presented which shows whether or not scroungers are maintained in a group, depending on their frequency and the group size. Some of the predictions of the model were tested in captive flocks of house sparrows Passer domesticus L. Here the scroungers obtained most of their food (mealworms) by interaction and the producers found most of their food by actively foraging: the pay-off to each type was measured as mealworm capture rate. Neither type changed strategy opportunistically in response to instantaneous flock composition but, not surprisingly, scroungers fared better when one of more producers were present. However, scrougers did much worse than expected when greatly outnumbered by producers, perhaps because producers then found the available food very quickly.     

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.     

Continuous cycling of grouped vs. solitary strategy frequencies in a predator-prey model

We present a model of predator and prey grouping strategies using game theory. As predators respond strategically to prey behavior and vice versa, the model is based on a co-evolution approach. Focusing on the "many eyes-many mouths" trade-off, this model considers the benefits and costs of being in a group for hunting predators and foraging prey: predators in a group have more hunting success than solitary predators but they have to share the prey captured; prey in a group face a lower risk of predation but greater competition for resources than lone prey. The analysis of the model shows that the intersections of four curves define distinct areas in the parameter space, corresponding to different strategies used by predators and prey at equilibrium. The model predictions are in accordance with empirical evidence that an open habitat encourages group living, and that low risks of predation favor lone prey. Under some conditions, continuous cycling of the relative frequencies of the different strategies may occur. In this situation, the proportions of grouped vs. solitary predators and prey oscillate over time.     

Co-evolution of learning complexity and social foraging strategies

Variation in learning abilities within populations suggests that complex learning may not necessarily be more adaptive than simple learning. Yet, the high cost of complex learning cannot fully explain this variation without some understanding of why complex learning is too costly for some individuals but not for others. Here we propose that different social foraging strategies can favor different learning strategies (that learn the environment with high or low resolution), thereby maintaining variable learning abilities within populations. Using a genetic algorithm in an agent-based evolutionary simulation of a social foraging game (the producer-scrounger game) we demonstrate how an association evolves between a strategy based on independent search for food (playing a producer) and a complex (high resolution) learning rule, while a strategy that combines independent search and following others (playing a scrounger) evolves an association with a simple (low resolution) learning rule. The reason for these associations is that for complex learning to have an advantage, a large number of learning steps, normally not achieved by scroungers, are necessary. These results offer a general explanation for persistent variation in cognitive abilities that is based on co-evolution of learning rules and social foraging strategies.     

Does prey size matter? Novel observations of feeding in the leatherback turtle (Dermochelys coriacea) allow a test of predator–prey size relationships

Optimal foraging models predict that large predators should concentrate on large prey in order to maximize their net gain of energy intake. Here, we show that the largest species of sea turtle, Dermochelys coriacea, does not strictly adhere to this general pattern. Field observations combined with a theoretical model suggest that a 300 kg leatherback turtle would meet its energetic requirements by feeding for 3-4 h a day on 4 g jellyfish, but only if prey were aggregated in high-density patches. Therefore, prey abundance rather than prey size may, in some cases, be the overriding parameter for foraging leatherbacks. This is a classic example where the presence of small prey in the diet of a large marine predator may reflect profitable foraging decisions if the relatively low energy intake per small individual prey is offset by high encounter rates and minimal capture and handling costs. This study provides, to our knowledge, the first quantitative estimates of intake rate for this species.