Carlos Bernstein

The ideal free distribution and predator-prey populations

The ideal free distribution, a theoretical model of the distribution of competitors between habitat patches, has recently undergone a number of modifications and extensions. These fall into two main categories: those that assume that equilibrium is attained, and those that establish whether it is attained. The modifications suggest ways in which behavioural properties of individuals might affect the distribution of competitors, and clear a path for further empirical tests.

Information acquisition and time allocation in insect parasitoids

Abstract All animals face the problem of finding resources for growth, maintenance and reproduction. Foraging in a heterogeneous (i.e. patchy) environment requires seemingly complex decisions, such as where to forage, and for how long. To make such decisions, animals need to acquire relevant information from their environment. Recent studies of how parasitoids acquire information and allocate their time to the exploitation of host patches use a combination of functional (evolutionary) and causal (mechanistic) approaches. They show that parasitoids can allocate foraging time to patches in an adaptive way and that members of the same species can respond differently to the same environmental cues, depending on their physiological state and previous experiences or on genetic differences. Functional models now help to explain these contrasting responses.

Food‐Searching in Parasitoids: The Dilemma of Choosing between ‘Immediate’ or Future Fitness Gains

Many parasitoid wasps and flies feed habitually on sugar-rich foods, consuming nectar and/or homopteran honeydew in the wild, and substitutes such as diluted honey in the laboratory. Consumption of these ‘non-host foods’ generally results in increases in female life expectancy, dispersal capacity, and realized fecundity. Typically in the wild, hosts and food sources are spatially separate. A female parasitoid therefore faces a choice as to which of the two types of resource she should forage for. Foraging for hosts will increase the likelihood of her obtaining ‘immediate’ fitness gains, but it will decrease her life expectancy. Foraging for food will postpone egg-laying to a later stage in adult life (constituting an ‘immediate’ reproductive opportunity cost), and will also incur energetic and mortality costs. However, it will increase opportunities to locate hosts in the future. From the standpoint of the fitness consequences of parasitoid foraging decisions, the exploitation of non-host foods is thus a highly interesting topic, posing the question of how females should forage so as to optimize trade-offs with respect to the use of both time and metabolic resources, and also mortality risks. In order to understand how such optimization might be achieved, we review current knowledge regarding resource ‘income’ and ‘capital’ used by females of parasitoid species that feed solely on non-host materials. Host-foraging versus non-host food-foraging, in such insects, has previously been modeled by means of stochastic dynamic programming. Using this technique, we model the behavioral scenario in which hosts and food patches are concurrently available but spatially separate. We focus initially on the egg maturation strategy of pro-ovigeny (in which all eggs are mature upon female emergence), but then examine the alternative and more common strategy of synovigeny (some eggs are immature). We discuss briefly the implications of variation in food availability for host population dynamics, and relate these to biological control scenarios. Finally, we identify promising avenues of future research. 9781405163477_4_007.qxd 03/09/2007 04:08PM Page 129

Energy dynamics in a parasitoid foraging in the wild

Although parasitoids are used widely as a biological models for understanding the evolution of animal behaviour, most studies have been constrained to the laboratory. The dearth of field studies has been compounded by the almost complete ignorance of the physiological parameters involved in foraging and dispersal, in particular of the energetic constraints imposed by resource limitation. We estimated the dynamics of carbohydrates and lipids reserves of Venturia canescens (Gravenhorst) females by releasing individuals of known nutritional status in a natural environment and recapturing them using host-containing traps. The recapture rate was around 30%. These results were compared with the reserves of caged animals kept under different experimental conditions (freshly emerged, starved to death, fed ad libitum and partially starved). Wild animals were also sampled in order to estimate the resource levels of the local population. The results show that: (i) wasps are able to maintain a nearly constant level of energy over an extended foraging period; (ii) V. canescens takes sugars in the field; and (iii) the lipid reserves accumulated during the larval life may be limiting as lipogenesis does not take place in adults even under conditions of high sugar availability. These results demonstrate that wasps can forage for hosts and food and disperse in this habitat for hours and days without running into a severe risk of energy limitation.

Behavioral Ecology of Insect Parasitoids

Many parasitoid wasps and flies feed habitually on sugar-rich foods, consuming nectar and/or homopteran honeydew in the wild, and substitutes such as diluted honey in the laboratory. Consumption of these ‘non-host foods’ generally results in increases in female life expectancy, dispersal capacity, and realized fecundity. Typically in the wild, hosts and food sources are spatially separate. A female parasitoid therefore faces a choice as to which of the two types of resource she should forage for. Foraging for hosts will increase the likelihood of her obtaining ‘immediate’ fitness gains, but it will decrease her life expectancy. Foraging for food will postpone egg-laying to a later stage in adult life (constituting an ‘immediate’ reproductive opportunity cost), and will also incur energetic and mortality costs. However, it will increase opportunities to locate hosts in the future. From the standpoint of the fitness consequences of parasitoid foraging decisions, the exploitation of non-host foods is thus a highly interesting topic, posing the question of how females should forage so as to optimize trade-offs with respect to the use of both time and metabolic resources, and also mortality risks. In order to understand how such optimization might be achieved, we review current knowledge regarding resource ‘income’ and ‘capital’ used by females of parasitoid species that feed solely on non-host materials. Host-foraging versus non-host food-foraging, in such insects, has previously been modeled by means of stochastic dynamic programming. Using this technique, we model the behavioral scenario in which hosts and food patches are concurrently available but spatially separate. We focus initially on the egg maturation strategy of pro-ovigeny (in which all eggs are mature upon female emergence), but then examine the alternative and more common strategy of synovigeny (some eggs are immature). We discuss briefly the implications of variation in food availability for host population dynamics, and relate these to biological control scenarios. Finally, we identify promising avenues of future research. 9781405163477_4_007.qxd 03/09/2007 04:08PM Page 129

Host and food searching in a parasitic wasp Venturia canescens : a trade-off between current and future reproduction?

Whether to invest in current or future reproduction is an important trade-off in life history evolution. For insect parasitoids, this trade-off is determined, among other factors, by the decision whether to search for hosts (immediate gain of fitness) or food (delayed fitness gains). Although host searching has been well studied, food sources, cues that parasitoids use to search for food and how insects modify their feeding behaviour have not. To address these questions, we investigated the food- and host-searching decisions made by the parasitoid Venturia canescens in both laboratory (olfactometer experiments) and field conditions (choice experiments). The wasps detected chemical cues associated with food, as well as those associated with hosts, and moved towards one or the other according to their nutritional state. Females used as food sources the same fruits that harboured hosts and detected the olfactory cues that would direct them to these fruits. Field results were consistent with those obtained in the laboratory. By integrating responses to infochemicals related to host and food, V. canescens might reduce the costs associated with food searching, so that more time and energy can be allocated to foraging for hosts. This behaviour should result in an adaptive advantage over parasitoids that incur additional costs by searching for hosts and food in different locations.

Predator Migration Decisions, the Ideal Free Distribution, and Predator‐Prey Dynamics

The aim of the present work is to analyze the influence of optimal predator emigration decisions that can lead to the ideal free distribution (IFD) on the stability of predator‐prey systems. The assumption of optimal decisions is then relaxed to analyze the possible influence of different degrees of deviation from the IFD. The first migration rule we analyze is based on the marginal‐value theorem and assumes perfect knowledge of capture rate in the patch of residence and in the environment as a whole. When migration rates are high, this rule leads the predator population to the IFD. The results suggest that under these conditions predator migration plays no major role in the stability of the system. This is so because the systems naturally merge into a single patch. This result is independent of the particular functional response used. The other two rules we analyze take into account lower migration rates, the limitations in making optimal decisions by predators, and the possible constraints in the assessment of intake rate in the different patches. The results suggest that the processes that hinder the convergence of the populations to the IFD might make a major contribution to the stability of the system.

Geographical distribution and genetic relatedness of sympatrical thelytokous and arrhenotokous populations of the parasitoid Venturia canescens (Hymenoptera)

Theory predicts that asexual reproduction has a competitive advantage over sexual reproduction because of the twofold cost of producing males. Few systems are suitable for directly testing this prediction. In the solitary parasitoid wasp Venturia canescens both arrhenotokously (sexual) and thelytokously (asexual) reproducing individuals occur sympatrically. We sampled 922 wasps from 22 localities along the coast of south‐eastern France. Thelytokous wasps were less abundant (23%) than arrhenotokous wasps and were almost always found in sympatry with arrhenotokous ones. An analysis of genetic relatedness using amplified fragment length polymorphism (AFLP) markers showed the existence of a widespread thelytokous clone. In addition, a few thelytokous individuals were found to be closely related to arrhenotokous ones and vice versa. These data suggest the occurrence of occasional gene flow between both reproductive modes and/or recurrent origin of thelytokous clones from coexisting arrhenotokous populations in the area. The results are discussed in the context of the paradox of sex.

Patch-Marking and Optimal Search Patterns in the Parasitoid Venturia canescens

We investigate whether Venturia canescens marks areas previously searched for hosts and the implication of this behaviour with respect to optimal search patterns. We show for the first time, that while searching on a host patch, V. canescens deposits a marking chemical on the surface of a patch. This marker influences both the behaviour of parasitoids subsequently visiting the patch and the within-patch search pattern of the foraging parasitoid. Individuals discriminate between the marks left by themselves or by conspecifics. Search is not fully systematic, as marked areas are frequently revisited. The adaptive significance of revisiting marked areas and the implications of systematic search on population dynamics are discussed.

The influence of temperature and host availability on the host exploitation strategies of sexual and asexual parasitic wasps of the same species

In the hymenopteran parasitoid Venturia canescens, asexual (obligate thelytoky not induced by Wolbachia bacteria) and sexual (arrhenotokous) wasps coexist in field conditions despite the demographic cost incurred due to the production of males by sexual females. Arrhenotoky predominates in field conditions, whereas populations in indoor conditions (mills, granaries) are exclusively thelytokous. These differences in the relative abundance of the two modes of reproduction between environments suggest that the individuals of each reproductive mode may have developed strategies adapted to the conditions prevailing in each kind of habitat. The two environments contrast in temperature variability and in the spatial heterogeneity of host availability. In this study, we considered the combined effect of temperature and host availability on host patch exploitation by thelytokous and arrhenotokous V. canescens. As expected, arrhenotokous females were more sensitive to temperature changes. If the temperature decreased before foraging, they remained longer and exploited patches more thoroughly. This is consistent with the expected behaviour of parasitoids in response to signs of unfavourable conditions that entail increasing risk of time limitation or a reduced probability of attaining further patches. Both arrhenotokous and thelytokous females increased patch exploitation with host availability. However, unexpectedly, we found no difference in the way the two types of wasp responded to differences in host availability. Differences in the strategies adopted under different environmental conditions may indicate divergence of niche-specific life history traits between the two modes of reproduction. Niche displacement may partly account for the coexistence of these two modes of reproduction at a geographical scale.