Stochasticity and controllability of nutrient sources in foraging: host‐feeding and egg resorption in parasitoids

Abstract

Abstract. The trade-off between current and future reproduction has led many organisms experiencing stochastic reproductive opportunities to be flexible in their resource acquisition and allocation rules. Many parasitoid wasps display flexibility in choosing to host-feed or oviposit on a host and possess an ovarian system enabling nutrient reallocation through egg resorption.The aim of this work is to assess the complementary adaptive values of host-feeding and egg resorption as functions of host density in a synovigenic (maturing eggs throughout its adult life) parasitoid, Eupelmus vuilleti (Hymenoptera: Eupelmidae), for which there is a uniquely large base of relevant knowledge. We developed a series of models of increasing complexity, starting from a simple analytical model without egg resorption and moving on to data-rich stochastic dynamic programming models (SDP), without and with resorption.The analytical model enabled the characterization of two, long-and short-term, foraging strategies which determine host usage. Oviposition is favored at low host densities (leading to the short-term strategy), while host-feeding is favored at high host densities (leading to the long-term strategy). The change of strategy occurs abruptly at intermediate host densities. The SPD models not only confirmed these predictions, but also identified smaller regions of decisions driven by day/night cycles and approaching death and predicted major shifts in daily activity patterns according to the chosen strategy. The fitness gain due to resorption is highest at intermediate host densities, where females adopt the riskier but more profitable long-term strategy. Such a result contrasts with the generally held view, which assumes highest gains at the lowest host densities. A counterintuitive result is the higher prevalence of host-feeding associated with the ability to resorb eggs.Considering egg resorption as a last-resort strategy is underestimating its adaptive value, which is best understood with reference to other sources of nutrients. Its deterministic and controllable nature acts as insurance to forage and oviposit at low host densities, despite irregular food availability and potential death through starvation. Thus timing, not so much overall energy gain, matters in egg resorption. The approach can be extended to other situations, and we highlight an unexpected analogy of our results with the hoarding behavior of vertebrates.

Does synovigeny confer reproductive plasticity upon a parasitoid wasp that is faced with variability in habitat richness?

“…To maximize their reproductive success in the face of environmental variation in availability of resources and reproductive opportunities, animals are expected to be flexible in the allocation of their limited set of physiological resources to functions associated with either reproduction or survival (Richard & Casas, 2009). Understanding the factors that constrain such allocation and so affect reproductive success, life histories, foraging behaviour, and population demographic features requires detailed insight into the processes of resource acquisition and allocation in different environments (Strand & Casas, 2008;Boggs, 2009).…”

Comparing resource exploitation and allocation of two closely related aphid parasitoids sharing the same host

“…The intimate physiological interaction between host and parasitoid larvae facilitates the evolution of specialized physiological traits to maximally exploit host resources (Price 1972;Vinson and Iwantsch 1980;Godfray 1994;Rivero et al 2001;Harvey and Strand 2002). Adult parasitoids are free-living and their reproductive opportunities are largely influenced by the number and the distribution of host resources in which they lay eggs (Godfray 1994;Rosenheim 1999;Rosenheim et al 2000;Richard and Casas 2009). As a result, parasitoids often evolved egg production strategies that closely reflect host availability (Ellers et al 2000;Ellers and Jervis 2004).…”

The Endocrine Basis for Reproductive Life-history Trade-offs during the Previtellogenic Resting Stage in the Yellow Fever Mosquito, Aedes aegypti

“…For example, studies that explored the differences in male/female survivorship during starvation have shown that the ability to resorb ovarian tissues provides a survival advantage to females but for obvious reasons no survival advantage was afforded to males which suggests that reproductive tissue can support survival directly (Ohgushi, 1996;. Other work has shown that resorption directly extends survival and can benefit long-term fecundity by sacrificing short-term fecundity (Boggs and Ross, 1993;Ohgushi, 1996;Richard and Casas, 2009;Rosenheim et al, 2000). On the surface, these examples seem to demonstrate that resorption represents a reversal of resources away from the germ and toward the soma.…”

“…In this species, the resorption of a single egg is only able to cover less than 10% of daily energy needs (Casas et al, 2005). In E. vuilleti as well as the mosquito, a simple relationship between nutrition and resorption is not clearly evident as resorbed eggs do not seem to be able to provide the kinds of benefits to survival that one would expect (Richard and Casas, 2009). Richard and Casas (2009) explain resorption as a buffer against stochasticity in the environment whereby a low value resource (ovarian follicles) can confer a fitness advantage primarily because of the controllability of this resource.…”

“…The redirection of reproductive nutrients to support alternative processes is supported by studies that explored the differences in female/male survivorship under starvation conditions which have demonstrated that the resources contained within the ovary can be a valuable nutrient store for females (and one unavailable to males) when dealing with environmental constraints (Ohgushi, 1996;. Other work has suggested that the nutritional resources recovered from the ovary can be used to improve survival, extend search time for resources or hosts, and maximize overall fitness (Boggs and Ross, 1993;Ohgushi, 1996;Richard and Casas, 2009;Rosenheim et al, 2000). Like many resource allocation decisions, the balance between nutrition, reproduction, and survival is likely to be mediated hormonally Trumbo and Robinson, 2004) Juvenile hormone (JH) has been suggested as the main hormonal factor that controls follicular resorption in some insects, a role that conveniently meshes with JH's broader participation in mediating resource allocation trade-offs (Reviewed in Bell and Bohm, 1975).…”