Anne Marie Cortesero

Impact of foliar herbivory on the development of a root-feeding insect and its parasitoid

The majority of studies exploring interactions between above- and below-ground biota have been focused on the effects of root-associated organisms on foliar herbivorous insects. This study examined the effects of foliar herbivory by Pieris brassicae L. (Lepidoptera: Pieridae) on the performance of the root herbivore Delia radicum L. (Diptera: Anthomyiidae) and its parasitoid Trybliographa rapae (Westwood) (Hymenoptera: Figitidae), mediated through a shared host plant Brassica nigra L. (Brassicaceae). In the presence of foliar herbivory, the survival of D. radicum and T. rapae decreased significantly by more than 50%. In addition, newly emerged adults of both root herbivores and parasitoids were significantly smaller on plants that had been exposed to foliar herbivory than on control plants. To determine what factor(s) may have accounted for the observed results, we examined the effects of foliar herbivory on root quantity and quality. No significant differences in root biomass were found between plants with and without shoot herbivore damage. Moreover, concentrations of nitrogen in root tissues were also unaffected by shoot damage by P. brassicae larvae. However, higher levels of indole glucosinolates were measured in roots of plants exposed to foliar herbivory, suggesting that the development of the root herbivore and its parasitoid may be, at least partly, negatively affected by increased levels of these allelochemicals in root tissues. Our results show that foliar herbivores can affect the development not only of root-feeding insects but also their natural enemies. We argue that such indirect interactions between above- and below-ground biota may play an important role in the structuring and functioning of communities.

Systemic Release of Herbivore-Induced Plant Volatiles by Turnips Infested by Concealed Root-Feeding Larvae Delia radicum L.

When attacked by herbivorous insects, many plants emit volatile compounds that are used as cues by predators and parasitoids foraging for prey or hosts. While such interactions have been demonstrated in several host–plant complexes, in most studies, the herbivores involved are leaf-feeding arthropods. We studied the long-range plant volatiles involved in host location in a system based on a very different interaction since the herbivore is a fly whose larvae feed on the roots of cole plants in the cabbage root fly, Delia radicum L. (Diptera: Anthomyiidae). The parasitoid studied is Trybliographa rapae Westwood (Hymenoptera: Figitidae), a specialist larval endoparasitoid of D. radicum. Using a four-arm olfactometer, the attraction of naive T. rapae females toward uninfested and infested turnip plants was investigated. T. rapae females were not attracted to volatiles emanating from uninfested plants, whether presented as whole plants, roots, or leaves. In contrast, they were highly attracted to volatiles emitted by roots infested with D. radicum larvae, by undamaged parts of infested roots, and by undamaged leaves of infested plants. The production of parasitoid-attracting volatiles appeared to be systemic in this particular tritrophic system. The possible factors triggering this volatile emission were also investigated. Volatiles from leaves of water-stressed plants and artificially damaged plants were not attractive to T. rapae females, while volatiles emitted by leaves of artificially damaged plants treated with crushed D. radicum larvae were highly attractive. However, T. rapae females were not attracted to volatiles emitted by artificially damaged plants treated only with crushed salivary glands from D. radicum larvae. These results demonstrate the systemic production of herbivore-induced volatiles in this host-plant complex. Although the emission of parasitoid attracting volatiles is induced by factors present in the herbivorous host, their exact origin remains unclear. The probable nature of the volatiles involved and the possible origin of the elicitor of volatiles release are discussed.

Intrinsic and extrinsic competitive interactions between two larval parasitoids of Heliothis virescens

1. Competition between parasitoid species may be a key factor in the community dynamics of plant–herbivore‐parasitoid systems and is an important consideration in the selection and management of effective biological control agents.

Comparisons and Contrasts in Host-Foraging Strategies of Two Larval Parasitoids with Different Degrees of Host Specificity

In theory, the degree of specificity of the signals a parasitoid species needs to successfully locate its host correlates with its level of specialization. We examined this question by comparing the foraging strategies of two parasitoids that differ in their host ranges. In wind-tunnel experiments, we investigated how systemically released herbivore-induced volatiles were used by the generalist parasitoid,Cotesia marginiventris (Cresson) and the specialist,Microplitis croceipes (Cresson). We determined the relative influence of these volatiles as compared to other signals emitted in the host orientation of the two parasitoids. Both the generalist and the specialist parasitoid strongly preferredSpodoptera exigua (Hübner) leaf-induced systemic plants over undamaged plants when no other information was available. When wasps were given a choice between leaf-induced and undamaged plants carrying other plant- or host-related materials, the responses differed for the two species.C. marginiventris appeared to cue primarily on recent damage volatiles, whereasM. croceipes appeared to cue primarily on host frass volatiles. However, recent damage on previously leaf-induced plants, was strongly preferred to recent damage on plants previously damaged by both species. When plants were induced at the squares byHelicoverpa zea (Boddie), onlyM. croceipes exhibited a preference for these plants over undamaged plants. The adaptive significance of the behaviors as related to dietary specializations of the parasitoids is discussed.

Parasitoid-specific induction of plant responses to parasitized herbivores affects colonization by subsequent herbivores

Plants are exposed to a suite of herbivorous attackers that often arrive sequentially. Herbivory affects interactions between the host plants and subsequently attacking herbivores. Moreover, plants may respond to herbivory by emitting volatile organic compounds (VOCs) that attract carnivorous natural enemies of the herbivores. However, information borne by VOCs is ubiquitous and may attract carnivores, such as parasitoids, that differ in their effectiveness at releasing the plant from its herbivorous attackers. Furthermore, the development of parasitoids within their herbivorous hosts, attacking a given host plant, may influence the elicitation of defensive reactions in the host plant. This may, in turn, affect the behavior of subsequent herbivores attacking the host plant. Here, we show that the species identity of a parasitoid had a more significant effect on defense responses of Brassica oleracea plants than the species identity of the herbivorous hosts of the parasitoids. Consequently, B. oleracea plants that were damaged by caterpillars (Pieris spp.) parasitized by different parasitoid species varied in the degree to which diamondback moths (Plutella xylostella) selected the plants for oviposition. Attracting parasitoids in general benefitted the plants by reducing diamondback moth colonization. However, the species of parasitoid that parasitized the herbivore significantly affected the magnitude of this benefit by its species-specific effect on herbivore–plant interactions mediated by caterpillar regurgitant. Our findings show that information-mediated indirect defense may lead to unpredictable consequences for plants when considering trait-mediated effects of parasitized caterpillars on the host plant and their consequences because of community-wide responses to induced plants.

Differences in volatile profiles of turnip plants subjected to single and dual herbivory above- and belowground.

Plants attacked by herbivorous insects emit volatile organic compounds that are used by natural enemies to locate their host or prey. The composition of the blend is often complex and specific. It may vary qualitatively and quantitatively according to plant and herbivore species, thus providing specific information for carnivorous arthropods. Most studies have focused on simple interactions that involve one species per trophic level, and typically have investigated the aboveground parts of plants. These investigations need to be extended to more complex networks that involve multiple herbivory above- and belowground. A previous study examined whether the presence of the leaf herbivore Pieris brassicae on turnip plants (Brassica rapa subsp. rapa) influences the response of Trybliographa rapae, a specialist parasitoid of the root feeder Delia radicum. It showed that the parasitoid was not attracted by volatiles emitted by plants under simultaneous attack. Here, we analyzed differences in the herbivore induced plant volatile (HIPV) mixtures that emanate from such infested plants by using Orthogonal Partial Least Squares-Discriminant Analysis (OPLS-DA). This multivariate model focuses on the differences between odor blends, and highlights the relative importance of each compound in an HIPV blend. Dual infestation resulted in several HIPVs that were present in both isolated infestation types. However, HIPVs collected from simultaneously infested plants were not the simple combination of volatiles from isolated forms of above- and belowground herbivory. Only a few specific compounds characterized the odor blend of each type of damaged plant. Indeed, some compounds were specifically induced by root herbivory (4-methyltridecane and salicylaldehyde) or shoot herbivory (methylsalicylate), whereas hexylacetate, a green leaf volatile, was specifically induced after dual herbivory. It remains to be determined whether or not these minor quantitative variations, within the background of more commonly induced odors, are involved in the reduced attraction of the root feeder’s parasitoid. The mechanisms involved in the specific modification of the odor blends emitted by dual infested turnip plants are discussed in the light of interferences between biosynthetic pathways linked to plant responses to shoot or root herbivory.

Identification of a Widespread Monomolecular Odor Differentially Attractive to Several Delia Radicum Ground-dwelling Predators in the Field

Dimethyl disulfide (DMDS) was identified as a major volatile constituent of Brassica napus roots heavily infested by Delia radicum, the cabbage root fly. Attractiveness of this widespread compound was tested in the field in a naturally complex odorous environment. By using an original setup especially designed for ground dwelling beetles, different concentrations of the pure molecule as well as attractiveness of the natural blend emitted by the rotten part of infested roots were tested simultaneously. The use of general linear model (GLM) statistics permitted us to finely discriminate the responses among the different treatments. The main predators of D. radicum (i.e., two staphylinids Aleochara bilineata and Aleochara bipustulata and carabid beetles of the genus Bembidion) were significantly attracted by DMDS, but responded in different ways to the natural blend and to the different concentrations tested. The dose–response curves were similar for the two staphylinids. However, whereas A. bilineata was more attracted by the natural volatile blend than by its preferred DMDS concentration, A. bipustulata was attracted as much by the natural blend as by its preferred DMDS concentration. Carabid beetles exhibited a different response. They were not attracted by the natural blend, but responded to a wider range of DMDS concentrations that included low concentrations that did not attract the staphylinid beetles. These results are discussed according to the potential resources searched by each taxon studied and their specificity for the resources. The possible use of DMDS for enhancing biological control of D. radicum is mentioned.

Kin discrimination and altruism in the larvae of a solitary insect

Kin selection theory predicts altruism between related individuals, which requires the ability to recognize kin from non-kin. In insects, kin discrimination associated with altruistic behaviour is well-known in clonal and social species but in very few solitary insects. Here, we report that the solitary larvae of a non-social insect Aleochara bilineata Gyll. (Coleoptera; Staphylinidae) show kin discrimination and sibling-directed altruistic behaviour. Larvae superparasitize more frequently the hosts parasitized by non-kin individuals than those hosts parasitized by siblings. Kin discrimination probably occurs by self-referent phenotype matching, where an individual compares its own phenotype with that of a non-familiar related individual, a mechanism rarely demonstrated in animals. The label used to recognize kin from non-kin corresponds to substances contained in the plug placed on the hosts by the resident larvae during the parasitization process. Kin competition induced by a limited larval dispersion may have favoured the evolution of kin recognition in this solitary species.

Effect of expected offspring survival probability on host selection in a solitary parasitoid

Optimal Foraging Theory predicts that parasitoid females should optimize their host selection to maximize their lifetime fitness gain and parasitize the most profitable hosts. In particular, in solitary parasitoids, females should avoid superparasitism, at least when sufficient unparasitized hosts are available. However, when unparasitized hosts are scarce, they should prefer, among already parasitized hosts, those that provide the best survival probability to their progeny, which depends on the age and the developmental stage of the first parasitoid.

Aboveground herbivory affects indirect defences of brassicaceous plants against the root feeder Delia radicum Linnaeus: laboratory and field evidence

1. Belowground herbivory has recently been shown to disrupt the host location behaviour of aboveground parasitoids and thereby impact plants indirect defences. Reverse interactions, on the other hand, have received little attention so far.