Root-associated entomopathogenic fungi manipulate host plants to attract herbivorous insects.

Root-associated entomopathogenic fungi (R-AEF) indirectly influence herbivorous insect performance. However, host plant-R-AEF interactions and R-AEF as biological control agents have been studied independently and without much attention to the potential synergy between these functional traits. In this study, we evaluated behavioral responses of cabbage root flies [Delia radicum L. (Diptera: Anthomyiidae)] to a host plant (white cabbage cabbage Brassica oleracea var. capitata f. alba cv. Castello L.) with and without the R-AEF Metarhizium brunneum (Petch). We performed experiments on leaf reflectance, phytohormonal composition and host plant location behavior (behavioral processes that contribute to locating and selecting an adequate host plant in the environment). Compared to control host plants, R-AEF inoculation caused, on one hand, a decrease in reflectance of host plant leaves in the near-infrared portion of the radiometric spectrum and, on the other, an increase in the production of jasmonic, (+)-7-iso-jasmonoyl-L-isoleucine and salicylic acid in certain parts of the host plant. Under both greenhouse and field settings, landing and oviposition by cabbage root fly females were positively affected by R-AEF inoculation of host plants. The fungal-induced change in leaf reflectance may have altered visual cues used by the cabbage root flies in their host plant selection. This is the first study providing evidence for the hypothesis that R-AEF manipulate the suitability of their host plant to attract herbivorous insects.

Spider Communities and Biological Control in Native Habitats Surrounding Greenhouses.

The promotion of native vegetation as a habitat for natural enemies, which could increase their abundance and fitness, is especially useful in highly simplified settings such as Mediterranean greenhouse landscapes. Spiders as generalist predators may also be involved in intra-guild predation. However, the niche complementarity provided by spiders as a group means that increased spider diversity may facilitate complementary control actions. In this study, the interactions between spiders, the two major horticultural pests, Bemisia tabaci and Frankliniella occidentalis, and their naturally occurring predators and parasitoids were evaluated in a mix of 21 newly planted shrubs selected for habitat management in a highly disturbed horticultural system. The effects of all factors were evaluated using redundancy analysis (RDA) and the generalized additive model (GAM) to assess the statistical significance of abundance of spiders and pests. The GAM showed that the abundance of both pests had a significant effect on hunter spider's abundance, whereas the abundance of B. tabaci, but not F. occidentalis, affected web-weavers' abundance. Ordination analysis showed that spider abundance closely correlated with that of B. tabaci but not with that of F. occidentalis, suggesting that complementarity occurs, and thereby probability of biocontrol, with respect to the targeted pest B. tabaci, although the temporal patterns of the spiders differed from those of F. occidentalis. Conservation strategies involving the establishment of these native plants around greenhouses could be an effective way to reduce pest populations outdoors.

Habitat selection of a parasitoid mediated by volatiles informing on host and intraguild predator densities.

To locate and evaluate host patches before oviposition, parasitoids of herbivorous insects utilize plant volatiles and host-derived cues, but also evaluate predator-derived infochemicals to reduce predation risks. When foraging in host habitats infested with entomopathogenic fungi that can infect both a parasitoid and its host, parasitoids may reduce the risk of intraguild predation (IGP) by avoiding such patches. In this study, we examined whether the presence of the entomopathogenic fungi Metarhizium brunneum and Beauveria bassiana in soil habitats of a root herbivore, Delia radicum, affects the behavior of Trybliographa rapae, a parasitoid of D. radicum. Olfactometer bioassays revealed that T. rapae avoided fungal infested host habitats and that this was dependent on fungal species and density. In particular, the parasitoid avoided habitats with high densities of the more virulent fungus, M. brunneum. In addition, host density was found to be important for the attraction of T. rapae. Volatiles collected from host habitats revealed different compound profiles depending on fungal presence and density, which could explain the behavior of T. rapae. We conclude that T. rapae females may use volatile compounds to locate high densities of prey, but also compounds related to fungal presence to reduce the risk of IGP towards themselves and their offspring.

Mortality risk from entomopathogenic fungi affects oviposition behavior in the parasitoid wasp Trybliographa rapae.

Biological control of pests in agroecosystems could be enhanced by combining multiple natural enemies. However, this approach might also compromise the control efficacy through intraguild predation (IGP) among the natural enemies. Parasitoids may be able to avoid the risk of unidirectional IGP posed by entomopathogenic fungi through selective oviposition behavior during host foraging. Trybliographa rapae is a larval parasitoid of the cabbage root fly, Delia radicum. Here we evaluated the susceptibility of D. radicum and T. rapae to two species of generalist entomopathogenic fungi, Metarhizium brunneum isolate KVL 04-57 and Beauveria bassiana isolate KVL 03-90. Furthermore, T. rapae oviposition behavior was assessed in the presence of these entomopathogenic fungi either as infected hosts or as infective propagules in the environment. Both fungi were pathogenic to D. radicum larvae and T. rapae adults, but with variable virulence. When host patches were inoculated with M. brunneum conidia in a no-choice situation, more eggs were laid by T. rapae in hosts of those patches compared to control and B. bassiana treated patches. Females that later succumbed to mycosis from either fungus laid significantly more eggs than non-mycosed females, indicating that resources were allocated to increased oviposition due to perceived decreased life expectancy. When presented with a choice between healthy and fungal infected hosts, T. rapae females laid more eggs in healthy larvae than in M. brunneum infected larvae. This was less pronounced for B. bassiana. Based on our results we propose that T. rapae can perceive and react towards IGP risk posed by M. brunneum but not B. bassiana to the foraging female herself and her offspring. Thus, M. brunneum has the potential to be used for biological control against D. radicum with a limited risk to T. rapae populations.