Patch Exploitation Strategies Research Articles

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.

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

AbstractThe 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.

The effect of direct interspecific competition on patch exploitation strategies in parasitoid wasps.

The presence of competitors may affect the pay-off of individuals' foraging strategies. They should therefore modify their resource exploitation decisions accordingly. In such a direct competition situation, theory predicts that individuals should stay longer on a resource patch than when foraging alone. However, models predicting patch residence time focus on intraspecific competition without agonistic interactions. Here, we investigate the patch use strategies of females of two parasitoid species, Eupelmus vuilleti and Dinarmus basalis, attacking the same host, Callosobruchus maculatus, knowing that D. basalis is more aggressive and can exclude E. vuilleti during pairwise contests for single hosts. Our results showed that time allocation and oviposition strategies differed in relation to the species and type of competition (i.e., presence/absence of competitor, simultaneous/sequential female introduction or resident/intruder female). Eupelmus vuilleti females tended to wait in the patch surroundings for D. basalis females' departure to return and exploit hosts parasitized by the opponent (after destruction of her eggs). In contrast, D. basalis females tended to self-superparasitize and stay motionless near the hosts. After detecting an E. vuilleti female entering the patch, they attacked and chased her permanently from the patch. Females of both species spent less time in the patch when faced with a competitor than when alone. This study is the first to test the influence of direct interspecific competition and arrival order on patch exploitation strategies in parasitoid species, and highlights the necessity to include agonistic behaviors in theoretical models predicting optimal patch residence time in competitive situations.

Patch exploitation strategies of parasitoids: The role of sex ratio and forager's interference in structuring metapopulations

We use a mathematical model to explore the effects of parasitoid reproductive strategies and foraging behavior in response to spatio-temporal variations in the patch quality of a host–parasitoid metapopulation system. The variations of patch quality over the landscape were measured by the presence of parasitoid competitors and the density of hosts. The parasitoid responses to patch quality are given by three different foraging behaviors: (i) the decision to remain in or leave the current patch; (ii) the control of progeny's sex ratio and (iii) competitive abilities, measured by changes in the potential to attack hosts due to interference from conspecifics in the exploited patch. We study the dynamics of host and parasitoid populations characterized by different levels of density-dependent sex ratio adjustment and interference competition. Our results show that population stability increases when parasitoid growth is correlated with patch conditions. The effect of sex ratio adjustment alone does not account for qualitative changes to system dynamics or to the distribution patterns of species. In contrast, the degree of competitive interference among the parasitoids plays a crucial role in constraining the parasitoids’ potential to reduce host populations and in determining the species’ distribution in the landscape. We found that high levels of interference competition disrupt the population dynamics within a patch and allows hosts to completely dominate the landscape. This study shows that the inclusion of life history traits and the co-evolutionary aspects of host–parasitoid interaction can help researchers to understand species distribution patterns in the landscape.

First in, last out: asymmetric competition influences patch exploitation of a parasitoid

Parasitoid females exploiting a patchy environment may encounter conspecifics on the host patches they visit or arrive in patches where other females have already parasitized hosts. When 2 or more foragers with differential arrivals exploit a resource patch simultaneously, the solution for the evolutionary stable patch residence times is the outcome of an asymmetric war of attrition. A theoretical prediction is that the forager that arrives first should stay longer than those arriving later, as a result of a resource value asymmetry. This study aims to examine how the arrival order on a host patch affects patch time in the solitary aphid parasitoid Aphidius ervi. For this purpose, 3 situations of competition were tested: single individuals foraging on unexploited patches (no competition), individuals foraging on previously exploited patches, and individuals exploiting patches in the presence of a competitor. Our data confirm the theoretical prediction: first-arriving females stay longer on a patch of hosts than second-arriving females. Neither host rejections nor host attacks affect patch-leaving decisions of females, but foraging with a competitor and previous encounters with a competitor increase the patch residence time of first-arriving females. This experiment is the first to test the effect of arrival order on patch exploitation strategies in nonfighting species. Key words: differential arrival, exploitative competition, foraging behavior, interference, parasitic wasp, war of attrition. [Behav Ecol]

Travel time affects optimal diets in depleting patches

Models of prey choice in depleting patches predict an expanding specialist strategy: Animals should start as specialists on the most profitable prey and then at some point during patch exploitation switch to a generalist foraging strategy. When patch residence time is long, the switch to a generalist diet is predicted to occur earlier than when patch residence time is short. We tested these predictions under laboratory conditions using female parasitoids (Aphidius colemani) exploiting patches of mixed instars aphid hosts (Myzus persicae, L1 and L4). The duration of patch exploitation was manipulated by changing travel time between patches. As predicted, patch residence times increase with travel time between patches. Our results provide empirical support for the expanding specialist prediction: Parasitoid females specialized initially on the more profitable hosts (L4), and as the patch depleted, they switched to a generalist diet by accepting more frequently the less profitable hosts (L1). The point at which they switched from specialist to generalist occurred later when travel times and hence patch residence times were short. By affecting the patch exploitation strategy, travel time also determines the composition of hosts left behind, the “giving up composition.” The change in the relative density of remaining host types alters aphid populations’ age structure.

Influence of environmental conditions on patch exploitation strategies of parasitoids

In patchy environments, patch-leaving decision rules are a key component of the foraging behavior of parasitoids that have to share their searching time between the different host patches to optimize the number of ovipositions. It has been experimentally shown that one of the proximate cues involved in patch-leaving decision is the number of ovipositions performed by the parasitoid while in the patch. Ovipositions can have either a decremental or an incremental effect on the patch residence time depending on parasitoid species. Previous theoretical studies have suggested that environmental conditions and the ability of parasitoids to reliably estimate the number of available hosts on a patch when entering it should influence how patch departure depends on ovipositions. We developed an individual-based model to test a large variety of patch-leaving decision rules in different environmental conditions. This model includes a more realistic representation of individual acquisition of information than previous theoretical work. In accordance with previous results, we show that the best use of information depends on environmental conditions. Moreover, we identify the environmental factors that have a decisive influence on the most appropriate type of rule (incremental or decremental). Decremental mechanisms are most efficient only in restricted conditions characterized by a large number of patches and few parasitoids. The sensitivity of decision rules to frequency-dependent processes was tested by numerical invasibility experiments. Rare mutants using any alternative rule never outperform populations using a high-performance rule. Incremental rules seem to be more sensitive than decremental ones to frequency-dependent processes. Key words: individual-based model, kairomone, optimal foraging, ovipositions, patch-leaving decisions, patchy environment. [Behav Ecol]

Patch exploitation strategy by an egg parasitoid in constant or variable environment

Abstract. 1. In this paper, the foraging behaviour (the proximal mechanisms involved in patch‐leaving rules and the egg dispersion) of an egg parasitoid, Anaphes victus, was analysed in environments containing either patches of constant quality (i.e. predictable environment) or patches of variable quality (i.e. unpredictable environment) in order to determine the motivational mechanisms used in patch‐leaving strategies.2. Comparison of the patch exploitation strategy of A. victus between the different habitats suggested that the response of A. victus to a given patch quality strongly depended on its past experiences. Females allocated more time and more eggs in a mixed quality patch after experiencing a poor quality patch than after experiencing a good quality patch. In a poor quality patch, females superparasitised more frequently after experiencing a poor quality patch than after experiencing a good quality patch. In a good quality patch, A. victus females laid more eggs after having visited two poor quality patches than after visiting good quality patches.3. Recent foraging experiences are used to estimate both the availability and spatial distribution of hosts in the environment and adjust foraging decisions accordingly. The observed variability in the patch‐leaving rules within the same species stresses the importance of previous experience when describing behaviours of female parasitoids.

Effect of low temperature exposure on oviposition behaviour and patch exploitation strategy in parasitic wasps

Learning of olfactory and gustatory cues occurs throughout the adult stage of parasitoids, particularly during host location and patch exploitation. A loss of learning capacities could affect both the whole host–parasitoid system and the wasps' reproductive success. We analysed the effect of low-temperature exposure on learning, patch exploitation strategies and patch-leaving rules used by Anaphes victus (Hymenoptera: Mymaridae). Females were stored 0, 3, 6 and 12 weeks at 4°C at the second larval instar. After emergence, females were offered three successive patches containing 16 hosts, of which 0, 50 and 100%, respectively, were parasitized, and their foraging behaviours were recorded. Cold-exposed females oviposited fewer eggs, seemed less able to learn external marks (or did not use their learning capacities), oviposited more in already parasitized hosts and used different patch-leaving rules to control females. The degree of the change in behaviour was positively correlated with the duration of cold exposure. Low-temperature exposure thus affected the reproductive success, expression of learning, host discrimination ability and patch-leaving decision rules of the parasitic wasps. We discuss the implications of these effects on the pattern of patch exploitation for biological control and field situations.

Patch exploitation strategies of parasitic wasps under intraspecific competition

The optimal residence time of a forager exploiting a resource patch in the absence of competitors has been much studied since the development of the marginal value theorem. However, several foragers are frequently observed exploiting the same patch simultaneously, and patch residence time has been surprisingly little studied in such competitive situations. The few theoretical models developed on this topic predict that foragers should engage in a war of attrition and stay in the patch longer than when foraging alone. We tested this prediction in Pachycrepoideus vindemmiae (Hymenoptera: Pteromalidae), a solitary parasitoid species in which females are known to defend the hosts they are exploiting via intraspecific fighting. By measuring the effect of direct (i.e., presence of conspecifics) and indirect (i.e., presence of already-parasitized hosts) competition on patch exploitation strategies, we revealed an apparent polymorphism of strategies. Indeed, in competitive situations, some members of the population tended to retreat almost immediately from the patch whereas other members tended to remain, further exploit the patch, and be more involved in interactions with conspecifics. The proportion of retreaters strongly depended on competition intensity and prior experience of competition. The forager's physiological state (age) also affects patch exploitation strategy and the intensity of interactions between competing females. Our results highlight the necessity for further theoretical studies that consider cases where contests between foragers are costly and take into account prior experience of competition and the forager's physiological state. Copyright 2005.

Superparasitism acceptance and patch-leaving mechanisms in parasitoids: a comparison between two sympatric wasps

Parasitoids often exploit hosts that have a clumped distribution. To divide their foraging effort between patches, females use encounters with unparasitized hosts as a source of information regarding local host density. Theory predicts that depending on host distribution, ovipositions should either increase (if the distribution is aggregated) or decrease (if the distribution is regular) the females' tendency to remain on the patch. However, patch time allocation theories usually ignore the possibility of superparasitism, even though it can change the predictions. We compared patch exploitation strategies of two related and sympatric Drosophila parasitoids. We investigated, with the Cox model, how females divide their foraging effort between patches of different densities and what proximal leaving mechanism they use. The species differed in the information input they used to adjust their patch time. Ovipositions decreased the patch-leaving tendency of Leptopilina heterotoma, which seldom superparasitized; this is consistent with previous results and with the aggregated distribution of Drosophila larvae. In contrast, no effect of oviposition was found on L. boulardi, which accepted most already parasitized hosts. Rejection of parasitized hosts increased the leaving tendency of L. heterotoma, but had no effect on L. boulardi. These wasps have thus evolved very different patch-leaving rules, possibly in response to differences in their superparasitism behaviour.

Can imperfect host discrimination explain partial patch exploitation in parasitoids?

Summary1. Host discrimination by Aphidius rhopalosiphi (De Stefani Perez) (Hymenoptera: Braconidae) was first studied on the grain aphid Sitobion avenae (Fabricius) (Homoptera: Aphididae). Females tended to avoid oviposition in hosts parasitised 3 h earlier. No evidence of host discrimination ability on freshly parasitised hosts was suggested, however, and ovipositional experience had no effect on host discrimination.2. The effects of host discrimination ability on the exploitation strategy of patches containing different proportions of unparasitised hosts and hosts parasitised for 3 h were studied. Females spent less time on patches with a higher proportion of parasitised hosts, reflecting the females' ability to perceive the potential profitability of the patch. This ability may be based on the nature of the hosts encountered (unparasitised or parasitised).3. Incomplete exploitation of unparasitised hosts was also observed. It seems that this partial exploitation is related to the inability of A. rhopalosiphi to recognise freshly parasitised hosts. As a female may experience a risk of self‐superparasitism during patch depletion, this could promote early departure from incompletely exploited patches.4. The effect of previous experience on the patch exploitation strategy was also assessed. Females were tested twice on two patches of the same quality. Results suggested that the experience acquired during a previous visit led the females to leave the patch sooner and to lay fewer eggs in parasitised hosts.5. Patch exploitation strategy may therefore be the result of different factors such as host discrimination and experience. The evolutionary consequences of the results are discussed.

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 conspecific females. On average, T. brassicae females spent more time on patches of higher quality, and all patches were reduced to the same level of profitability before being left. This appeared to be in accordance to the optimal predictions of the Charnov Marginal Value Theorem. The proximate leaving mechanisms involved were 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 rejection of a healthy host or of a host that was previously attacked by the same female (i.e., self-superparasitism) had a decremental effect. These patch leaving mechanisms did not change according to the quality of the patch the females were exploiting. A Monte Carlo simulation was developed around the results of the Cox regression model. The results suggest that this set of patch leaving rules seems to provide the females with a sufficient way to reach the predictions of the Charnov model. Among the different mechanisms involved, the incremental effect associated with each oviposition in a healthy host appeared to play the most important role. The relationship between the proximate mechanistic rules adopted by the females and the ultimate prediction of the Charnov model is discussed. Key words: patch leaving rules, Marginal Value Theorem, Cox regression model, parasitoids, Trichogramma, Monte Carlo simulation. [Behav Ecol 11:577–586 (2000)]

Load Size Variation in the Eastern Chipmunk, Tamias striatus: The Importance of Distance from Burrow and Canopy Cover

AbstractWe examined the degree to which chipmunks foraging from dishes containing sunflower seeds varied cheek pouch load size according to both travel time (distance from burrows) and predation hazard (canopy cover). Results showed that larger loads were taken under cover at some distance from burrows than were taken from closer or more open sites. Distance effects appeared to reflect the influence of traveling times on quitting harvest rates as predicted by central place foraging models. Quitting harvest rates also appeared to be higher under low than under dense canopy cover; this trend was most pronounced at some distance from burrows suggesting that foraging decisions were made relative to both energetics and predator avoidance. Chipmunks appeared to employ a patch exploitation strategy that minimized the hazard:gain ratio.