Patch exploitation strategies of parasitoids under indirect intra‐ and inter‐specific competition

1. Insect parasitoids are expected to evolve behavioural strategies to exploit resources in competitive environments optimally. Indirect competition between parasitoids is particularly common because exploited host patches remain available in the environment for other foraging individuals. 2. The effects of indirect competition on the behaviour of two closely related generalist egg parasitoids were investigated: Trichogramma pintoi Voegelé and Trichogramma minutum Riley (Hymenoptera: Trichogrammatidae). Patch residence time, a patch‐leaving mechanism, and progeny sex allocation of females foraging were analysed: (i) alone, (ii) in patches partially parasitised by conspecifics, and (iii) in patches partially parasitised by heterospecifics. 3. Each species responded differently to indirect competition. Trichogramma pintoi females shortened their patch residence times, but they did not adjust their progeny sex ratios. In contrast, T. minutum females did not modify their patch residence times, but they did increase their progeny sex ratios in response to competition. Both Trichogramma species used host rejection, either by antenna rejection or by ovipositor rejection, as a patch‐leaving mechanism. 4. In agreement with a companion study of direct competition using the same model species, the present results indicate that even amongst closely related species, responses to competition can vary considerably.     

Maintaining social cohesion is a more important determinant of patch residence time than maximizing food intake rate in a group-living primate,Japanese macaque (Macaca fuscata)

Animals have been assumed to employ an optimal foraging strategy (e.g., rate-maximizing strategy). In patchy food environments, intake rate within patches is positively correlated with patch quality, and declines as patches are depleted through consumption. This causes patch-leaving and determines patch residence time. In group-foraging situations, patch residence times are also affected by patch sharing. Optimal patch models for groups predict that patch residence times decrease as the number of co-feeding animals increases because of accelerated patch depletion. However, group members often depart patches without patch depletion, and their patch residence time deviates from patch models. It has been pointed out that patch residence time is also influenced by maintaining social proximity with others among group-living animals. In this study, the effects of maintaining social cohesion and that of rate-maximizing strategy on patch residence time were examined in Japanese macaques (Macaca fuscata). I hypothesized that foragers give up patches to remain in the proximity of their troop members. On the other hand, foragers may stay for a relatively long period when they do not have to abandon patches to follow the troop. In this study, intake rate and foraging effort (i.e., movement) did not change during patch residency. Macaques maintained their intake rate with only a little foraging effort. Therefore, the patches were assumed to be undepleted during patch residency. Further, patch residence time was affected by patch-leaving to maintain social proximity, but not by the intake rate. Macaques tended to stay in patches for short periods when they needed to give up patches for social proximity, and remained for long periods when they did not need to leave to keep social proximity. Patch-leaving and patch residence time that prioritize the maintenance of social cohesion may be a behavioral pattern in group-living primates.     

Knowing your habitat: linking patch-encounter rate and patch exploitation in parasitoids

According to optimal foraging theory, animals should decidewhether or not to leave a resource patch by comparing the currentprofitability of the patch with the expected profitability ofsearching elsewhere in the habitat. Although there is abundantevidence in the literature that foragers in general are wellable to estimate the value of a single resource patch, theirdecision making has rarely been investigated with respect tohabitat quality. This is especially true for invertebrates.We have conducted experiments to test whether parasitic waspsadjust patch residence time and exploitation in relation tothe abundance of patches within the environment. We used thebraconid Asobara tabida, a parasitoid of Drosophila larvae,as our model species. Our experiments show that these waspsreduce both the residence time and the degree of patch exploitationwhen patches become abundant in their environment, as predictedby optimal foraging models. Based upon a detailed analysis ofwasp foraging behavior, we discuss proximate mechanisms thatmight lead to the observed response. We suggest that parasitoidsuse a mechanism of sensitization and desensitization to chemicalsassociated with hosts and patches, in order to respond adaptivelyto the abundance of patches within their environment.     

Patch exploitation by non‐aggressive parasitoids under intra‐ and interspecific competition

The behavioral strategies evolved by insect parasitoids to optimize their foraging efforts have been the subject of many theoretical and empirical studies. However, the effects competition may have on these strategies, especially for species that do not engage in antagonistic behaviors, have received little attention. The objective of this study was to evaluate the effects of intraspecific and interspecific competition on patch exploitation strategies by two non‐aggressive species, Trichogramma pintoi Voegelé and Trichogramma minutum Riley (Hymenoptera: Trichogrammatidae), both generalist egg parasitoids. We analyzed the patch residence times of females, their patch‐leaving mechanisms, and the sex allocation of their progeny while foraging either alone, with an intraspecific competitor, or with an interspecific competitor. To some extent, each species responded differently to the presence of a competitor in the patch. Trichogramma pintoi females did not change their patch‐leaving mechanisms in response to competition and behaved as if under an exploitative competition regime, whereas T. minutum females did change their patch‐leaving mechanisms in response to competition and remained longer in the host patch than expected. Antennal rejection, and not oviposition, was the proximate behavioral mechanism underlying patch‐leaving decisions by both species. Neither species adjusted the sex allocation of their progeny in response to competition. These results indicate that the effects of competition differ even among closely related parasitoid species.     

Does group foraging promote efficient exploitation of resources?

Increased avoidance of food patches previously exploited by other companions has been proposed as one adaptive benefit of group foraging. However, does group foraging really represent the most efficient way to exploit non- or slowly-renewing resources? Here, I used simulations to explore the costs and benefits of exploiting non-renewing resources by foragers searching for food patches independently or in groups in habitats with different types of resource distribution. Group foragers exploited resources in a patch more quickly and therefore spent proportionately more time locating new patches. Reduced avoidance of areas already exploited by others failed to overcome the increased time cost of searching for new food patches and group foragers thus obtained food at a lower rate than solitary foragers. Group foraging provided one advantage in terms of a reduction in the variance of food intake rate. On its own, reduced avoidance of exploitation competition through group foraging appears unlikely to increase mean food intake rate when exploiting non-renewing patches but may provide a way to reduce the risk of an energy shortfall.     

Patch leaving decision rules and the Marginal Value Theorem: an experimental analysis and a simulation model

The patch exploitation strategy of females of the insect parasitoid Trichogramma brassicae was studied on patches containing different proportions of hosts that were previously attacked by conspecificfemales. On average, T. brassicae females spent more time onpatches of higher quality, and all patches were reduced tothe same level of profitability before being left. This appearedto be in accordance to the optimal predictions of the CharnovMarginal Value Theorem. The proximate leaving mechanisms involvedwere analyzed by means of a Cox proportional hazards model.Each oviposition in a healthy host appeared to have an incremental influence on the patch residence time, whereas each rejectionof a healthy host or of a host that was previously attackedby the same female (i.e., self-superparasitism) had a decrementaleffect. These patch leaving mechanisms did not change accordingto the quality of the patch the females were exploiting. AMonte Carlo simulation was developed around the results of the Cox regression model. The results suggest that this set of patchleaving rules seems to provide the females with a sufficientway to reach the predictions of the Charnov model. Among thedifferent mechanisms involved, the incremental effect associatedwith each oviposition in a healthy host appeared to play the most important role. The relationship between the proximatemechanistic rules adopted by the females and the ultimate predictionof the Charnov model is discussed.     

State dependent behavior and the Marginal Value Theorem

The Marginal Value Theorem (MVT) is the dominant paradigm inpredicting patch use and numerous tests support its qualitativepredictions. Quantitative tests under complex foraging situationscould be expected to be more variable in their support becausethe MVT assumes behavior maximizes only net energy-intake rate.However across a survey of 26 studies, foragers rather consistently"erred" in staying too long in patches. Such a consistent directionto the errors suggests that the simplifying assumptions ofthe MVT introduce a systematic bias rather than just imprecision. Therefore, I simulated patch use as a state-dependent responseto physiological state, travel cost, predation risk, prey densities,and fitness currencies other than net-rate maximization (e.g.,maximizing survival, reproductive investment, or mating opportunities).State-dependent behavior consistently results in longer patchresidence times than predicted by the MVT or another foragingmodel, the minimize µ/g rule, and these rules fail to closely approximate the best behavioral strategy over a widerange of conditions. Because patch residence times increasewith state-dependent behavior, this also predicts mass regulationbelow maximum energy capacities without direct mass-specificcosts. Finally, qualitative behavioral predictions from theMVT about giving-up densities in patches and the effects oftravel costs are often inconsistent with state-dependent behavior.Thus in order to accurately predict patch exploitation patterns,the model highlights the need to: (1) consider predator behavior(sit-and-wait versus actively foraging); (2) identify activitiesthat can occur simultaneously to foraging (i.e., mate searchor parental care); and (3) specify the range of nutritional states likely in foraging animals. Future predictive modelsof patch use should explicitly consider these parameters.     

Patch Time Allocation by a Parasitoid: The Influence of Con-specifics,Host Abundance and Distance to the Patch

Patch residence time is at the core of models of decision making by foragers living in patchy environments. We studied patch residence time (PRT) of Ibalia leucospoides, a parasitoid of the woodwasp Sirex noctilio, as assigned to 4 treatments (recent feeding and/or oviposition experience) foraging in an array of host-infested pine logs. We tested the effects of distance from release point, host abundance, and the number of con-specifics at the time of arrival, on patch (pine log) residence time. PRT depended on a combination of patch quality (number of hosts in a log) and distance from the release point. Neither the presence of con-specifics on the patch, prior exposure to hosts, nor feeding prior to the experiment affected the time spent on a patch. We conclude that PRT in I. leucospoides meets Marginal Value Theorem predictions qualitatively, overruling the effects recent oviposition experience, access to food and contact with conspecifics. These findings are in line with the reported pro-ovigeny in I. leucospoides as well as the strong spatial aggregation of hosts in the field.     

Interference competition,payoff asymmetries,and the social relationships of central place foragers

We present a central place foraging model that shows how payoff asymmetries originate in contests for access to resources. The essence of the model is that interference competition at resource points lowers the rate at which foragers can load prey, thereby depressing the rate of food delivery to the central place. We show that interference leads to asymmetric payoffs when contests involve foragers with (i) unequal travel distances between the central place and the contested resource points; (ii) inequalities in the rate of food delivery available from alternative foraging sites; (iii) differences in loading efficiency; or (iv) different abilities to interfere. We use the asymmetries to predict dominance rankings, and the patch exploitation tactics of individual foragers. We also consider the implications of the model for changes in the travel distance (= area) over which foragers can exclude competitors (= territoriality) as food density changes. Finally, incorporation of interference permits our model to predict the transition between scramble and contest competition.     

An experimental design and a statistical analysis separating interference from exploitation competition

Previous experimental studies of competition among foragers rarely distinguished between exploitation and interference competition. In many systems this separation is experimentally impossible without interfering with the natural behavior of the animals. Consequently, these studies can only demonstrate the combined effect of interference and exploitation on the forager’s feeding rate, namely, it usually decreases in a decelerating rate as a function of density. We suggest here a simple experimental and statistical procedure that facilitates the separation of the effects of interference from those of exploitation. This procedure includes manipulation of both predator density and the foraging experiment duration. The statistical analysis is based on multiple linear regression. The working assumption is that exploitation can be neglected at the beginning of the foraging experiment because, initially, predators do not experience diminishing returns in prey capture rates. Using both the results of an individual-based simulation and a field experiment dataset of gerbils foraging for seeds in an artificial food patch located in the field, we demonstrate that our procedure can successfully detect and separate the effect of interference from the combined overall effect of competition (i.e., interference plus exploitation). Inon Scharf and Ido Filin contributed equally to this paper.     

Optimal Bayesian foraging policies and prey population dynamics-some comments on Rodriguez-Girones and Vasquez

In this paper we show the density-dependent harvest rates of optimal Bayesian foragers exploiting prey occurring with clumped spatial distribution. Rodríguez-Gironés and Vásquez (1997) recently treated the issue, but they used a patch-leaving rule (current value assessment rule) that is not optimal for the case described here. An optimal Bayesian forager exploiting prey whose distribution follows the negative binomial distribution should leave a patch when the potential (and not instantaneous) gain rate in that patch equals the best long-term gain rate in the environment (potential value assessment rule). It follows that the instantaneous gain rate at which the patches are abandoned is an increasing function of the time spent searching in the patch. It also follows that the proportion of prey harvested in a patch is an increasing sigmoidal function of the number of prey initially present. In this paper we vary several parameters of the model to evaluate the effects on the forager's intake rate, the proportion of prey harvested per patch, and the prey's average mortality rate in the environment. In each case, we study an intake rate maximizing forager's optimal response to the parameter changes. For the potential value assessment rule we find that at a higher average prey density in the environment, a lower proportion of the prey is taken in a patch with a given initial prey density. The proportion of prey taken in a patch of a given prey density also decreases when the variance of the prey density distribution is increased and if the travel time between patches is reduced. We also evaluate the effect of using predation minimization, rather than rate maximization, as the currency. Then a higher proportion of the prey is taken for each given initial prey density. This is related to the assumption that traveling between patches is the most risky activity. Compared to the optimal potential value assessment rule, the current value assessment rule performs worse, in terms of long-term intake rate achieved. The difference in performance is amplified when prey density is high or highly aggregated. These results pertain to the foraging patch spatial scale and may have consequences for the spatial distribution of prey in the environment.     

Integrating the roles of information and competitive ability on the spatial distribution of social foragers

Understanding and predicting the spatial distribution of social foragers among patchily distributed resources is a problem that has been addressed with numerous approaches over the 30 yr since the ideal free distribution (IFD) was first introduced. The two main approaches involve perceptual constraints and unequal competitors. Here we present a model of social foragers choosing among resource patches. Each forager makes a probabilistic choice on the basis of the information acquired through past foraging experiences. Food acquisition is determined by the forager's competitive ability. This model predicts that perceptual constraints have a greater influence on the spatial distribution of foragers than unequal competitive abilities but that competitive ability plays an important role in determining an individual's information state and behavior. Better competitors have access to more information; consequently, we find that competitive abilities and perceptual constraints are integrated through the social environment occupied by individual foragers. Relative competitive abilities influence the forager's information state, and the ability to use information determines the resulting spatial distribution.     

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     

Preference in patchy landscapes: the influence of scale-specific intake rates and variance in reward

Understanding the responses of foragers to patchy distributionsof resources has formed a fundamental challenge in behavioralecology. Two currencies have been used to assess the patch preferencesof herbivores—intake rate maximization and risk sensitivity.We wished to understand if small mammalian foragers, collaredlemmings (Dichrostonyx groenlandicus), choose patches to maximizefood intake rate or to reduce risk of starvation in "variable"environments. Moreover, we examined the possibility that maximizingintake rate depends on the spatial scale of patchiness. We designedan experiment offering two alternative patches of food, varyingthe predictability of food rewards and the "potential intakerate" at different spatial scales. Collared lemmings did notconsistently select patches that maximized their intake rateat either scale studied. Instead, they chose patches offeringthe least variation in food reward over the course of the experiment.Collared lemmings used prior knowledge gained from previousforaging bouts to assess food variability. We interpret theseresults as evidence for risk-averse foraging strategies, whichare predicted for continuous foragers aiming to minimize riskof starvation.     

Optimal Bayesian Foraging Policies and Prey Population Dynamics—Some Comments on Rodríguez-Gironés and Vásquez

In this paper we show the density-dependent harvest rates of optimal Bayesian foragers exploiting prey occurring with clumped spatial distribution. Rodríguez-Gironés and Vásquez (1997) recently treated the issue, but they used a patch-leaving rule (current value assessment rule) that is not optimal for the case described here. An optimal Bayesian forager exploiting prey whose distribution follows the negative binomial distribution should leave a patch when the potential (and not instantaneous) gain rate in that patch equals the best long-term gain rate in the environment (potential value assessment rule). It follows that the instantaneous gain rate at which the patches are abandoned is an increasing function of the time spent searching in the patch. It also follows that the proportion of prey harvested in a patch is an increasing sigmoidal function of the number of prey initially present. In this paper we vary several parameters of the model to evaluate the effects on the forager's intake rate, the proportion of prey harvested per patch, and the prey's average mortality rate in the environment. In each case, we study an intake rate maximizing forager's optimal response to the parameter changes. For the potential value assessment rule we find that at a higher average prey density in the environment, a lower proportion of the prey is taken in a patch with a given initial prey density. The proportion of prey taken in a patch of a given prey density also decreases when the variance of the prey density distribution is increased and if the travel time between patches is reduced. We also evaluate the effect of using predation minimization, rather than rate maximization, as the currency. Then a higher proportion of the prey is taken for each given initial prey density. This is related to the assumption that traveling between patches is the most risky activity. Compared to the optimal potential value assessment rule, the current value assessment rule performs worse, in terms of long-term intake rate achieved. The difference in performance is amplified when prey density is high or highly aggregated. These results pertain to the foraging patch spatial scale and may have consequences for the spatial distribution of prey in the environment.     

Conspecific Avoidance During Foraging in Venturia canescens (Hymenoptera: Ichneumonidae): The Roles of Host Presence and Conspecific Densities

We explored the effects of the presence of conspecifics on host patch choice decisions made by the parasitoid Venturia canescens. Different odor sources were located in plastic boxes at the end of each arm of a glass Y-tube olfactometer. In a set of experiments, odor sources were either (a) host kairomone patches with or without conspecifics (5 or 20) or (b) two odor sources located in successive boxes (a host kairomone patch and a patch with 20 conspecifics in one arm versus a host patch and an empty patch in the other). Our results indicate that V. canescens avoids competition only at high conspecific densities. Avoidance occurs only when foraging wasps perceive the combined odors from host kairomones and conspecific females. Separating the host patch from conspecific parasitoids does not perturb avoidance behavior.     

The use and misuse of public information by foraging red crossbills

Group foragers may assess patch quality more efficiently bypaying attention to the sampling behavior of group members foragingin the same patch (i.e., using "public information"). To determinewhether red crossbills (Loxia curvirostra) use public informationto aid their patch departure decisions, we conducted experimentsthat compared the sampling behavior of crossbills foraging ona two-patch system (one patch was always empty, one patch containingseeds) when alone, in pairs, and in flocks of three. When foragingalone, crossbills departed from empty patches in a way thatwas qualitatively consistent with energy maximization. We foundevidence for the use of public information when crossbills werepaired with two flock mates, but not when paired with one flockmate. When foraging with two flock mates, crossbills sampledapproximately half the number of cones on the empty patch beforedeparting as compared to when solitary. Furthermore, as expected ifpublic information is used, the variance in both the numberof cones and time spent on the empty patch decreased when crossbillsforaged with two flock mates as compared to when alone. Althoughhigh frequencies of scrounging reduce the availability of publicinformation, scrounging is usually uncommon in crossbills, apparentlybecause they exploit divisible patches. Consequently, publicinformation is likely to be important to crossbills in the wild.We also show that feeding performance is greatly diminishedwhen the feeding performances of flock mates differ. This providesa mechanism that will favor assortative grouping by phenotypewhen phenotypes affect feeding performance, which may in turnpromote speciation in some groups of animals.     

Skuas at penguin carcass: patch use and state-dependent leaving decisions in a top-predator

Foraging decisions depend not only on simple maximization of energy intake but also on parallel fitness-relevant activities that change the forager's 'state'. We characterized patch use and patch leaving rules of a top-predatory seabird, the Brown Skua (Catharacta antarctica lonnbergi), which during its reproductive period in the Antarctic establishes feeding territories in penguin colonies. In feeding trials, we observed how skuas foraged at penguin carcass patches and analysed patch leaving decisions by incorporating the estimated state of foraging birds and patch availability.Patches were exploited in a characteristic temporal pattern with exponentially decreasing remaining patch sizes (RPSs) and intake rates. Patch size decreased particularly fast in small compared to large patches and exploitation ended at a mean RPS of 47.6% irrespective of initial size.We failed to identify a measure which those birds equalized upon patch departure from raw data. However, when accounting for the birds' state, we ascertained remaining patch size and intake rates to have the lowest variance at departure whereas food amount and feeding time remained variable. Statistical correction for territory size only and combined with state had lower effects, but remaining patch size remained the measure with lowest coefficient of variation. Thus, we could clearly reject a fixed-time or fixed-amount strategy for territorial skuas and rather suggest a state-dependent strategy that equalizes remaining patch size. Thus our results provide evidence that under natural conditions, territorial skuas adjust their foraging decision on actual energy requirements, i.e. offspring number and age.     

Male-male Competition and Reproductive Success in Elephant Seals

Male-male competition and reproductive success of northern elephantseals, Mirounga augustirostris, was studied for six consecutivebreeding seasons at Año Nuevo Island, California. Theconclusions were as follows: (i) Less than one third of themales in residence copulate during a breeding season. A fewmales are responsible for the majority of copulations, (ii)The number and age of males copulating varies with: (a) haremlocation and topography, (b) the number of estrous females inthe harem, and (c) the number of males competing for females,(iii) Copulation frequency is related directly to success inmale-male competition, i.e., social rank. (iv) The same individualsmay dominate breeding for three consecutive breeding seasons.(v) Successful males die within a year or two after their reproductivepeak. (vi) The reproductive success of most males is nil orlow because many die before reaching breeding age and some ofthose that reach maturity are prevented from mating by the highestranking males. (vii) Individual strategies have important consequencesfor reproductive success, (viii) Male-male competition is amajor cause of pup mortality prior to weaning. The potential reproductive success of males is much greaterthan that of females. Changes in colony number and compositionaffect the reproductive success of males as well as females.     

Local and neighboring patch conditions alter sex‐specific movement in banana weevils

Understanding the mechanisms underlying the movements and spread of a species over time and space is a major concern of ecology. Here, we assessed the effects of an individual's sex and the density and sex ratio of conspecifics in the local and neighboring environment on the movement probability of the banana weevil, Cosmopolites sordidus. In a “two patches” experiment, we used radiofrequency identification tags to study the C. sordidus movement response to patch conditions. We showed that local and neighboring densities of conspecifics affect the movement rates of individuals but that the density‐dependent effect can be either positive or negative depending on the relative densities of conspecifics in local and neighboring patches. We demonstrated that sex ratio also influences the movement of C. sordidus, that is, the weevil exhibits nonfixed sex‐biased movement strategies. Sex‐biased movement may be the consequence of intrasexual competition for resources (i.e., oviposition sites) in females and for mates in males. We also detected a high individual variability in the propensity to move. Finally, we discuss the role of demographic stochasticity, sex‐biased movement, and individual heterogeneity in movement on the colonization process.