Chemical Cues From Honeydew and Cuticular Extracts of Trialeurodes Vaporariorum Serve as Kairomones for The Parasitoid Encarsia Formosa.

Kairomones are semiochemicals that are emitted by an organism and which mediate interspecific interaction that is of benefit to an organism of another species that receives these chemical substances. Parasitoids find and recognize their hosts through eavesdropping on the kairomones emitted from the by-products or the body of the host. Hemipteran insect pests feed on plant sap and excrete the digested plant materials as honeydew. Honeydew serves as a nutritional food source for parasitoids and a medium for micro-organisms whose activity induces the release of volatiles exploited by parasitoids for host location. The parasitoid Encarsia formosa preferentially parasitizes its host, the greenhouse whitefly, Trialeurodes vaporariorum, on tomato Solanum lycopersicum, but little is known about the chemicals that mediate these interactions. We investigated the olfactory responses of the parasitoid E. formosa to odours from honeydew and nymphs of T. vaporariorum in a Y-tube olfactometer. Arrestment behaviour of the parasitoid to honeydew and nymph extracts, as well as to synthetic hydrocarbons, was also observed in Petri-dish bioassays. We found that T. vaporariorum honeydew volatiles attracted the parasitoid E. formosa but odours from the whitefly nymphs did not. We also found that the parasitoid spent more time searching on areas treated with extracts of honeydew and nymphs than on untreated areas. Gas-chromatography-mass spectrometric analysis revealed that the honeydew volatiles contained compounds such as (Z)-3-hexenol, δ-3-carene, 3-octanone, α-phellandrene, methyl salicylate, ß-ocimene, ß-myrcene, and (E)-ß-caryophyllene which are known to be attractive to E. formosa. The cuticular extracts of the nymphs predominantly contained alkanes, alkenes, and esters. Among the alkanes, synthetic nonacosane arrested the parasitoid. Our findings are discussed in relation to how the parasitoid E. formosa uses these chemicals to locate its host, T. vaporariorum.

Terpenes from herbivore-induced tomato plant volatiles attract Nesidiocoris tenuis (Hemiptera: Miridae), a predator of major tomato pests.

BACKGROUND: Biological control plays a key role in reducing crop damage by Tuta absoluta (Meyrick) and Trialeurodes vaporariorum (Westwood), which cause huge yield losses in tomato (Solanum lycopersicum L.). The mirid predator Nesidiocoris tenuis (Reuter) preys heavily on these pests, with satisfying control levels in tomato greenhouses. Although N. tenuis is known to be attracted to volatiles of tomato plants infested by T. absoluta and whitefly, little is known about the specific attractive compounds and the effect of prey density on the predator response. RESULTS: Y-tube olfactometer bioassays revealed that the attraction of N. tenuis to tomato volatiles was positively correlated with the density of T. absoluta infestation, unlike T. vaporariorum infestation. The predator was also attracted to volatiles of T. absoluta larval frass, but not to T. vaporariorum honeydew or T. absoluta sex pheromone. Among the herbivore-induced plant volatiles (HIPVs) that characterised the attractive plants infested with 20 T. absoluta larvae, olfactometer bioassays revealed that N. tenuis is attracted to the monoterpenes α-pinene, α-phellandrene, 3-carene, ß-phellandrene and ß-ocimene, whereas (E)-ß-caryophyllene was found to repel the predator. In dose-response bioassays, the five-component blend of the attractants elicited a relatively low attraction in the predator, and removal of ß-phellandrene from the blend enhanced the attraction of the predator to the resulting four-component blend, suggesting synergism among four monoterpenes. CONCLUSION: These findings suggest that a four-component blend of α-pinene, α-phellandrene, 3-carene and ß-ocimene could be used as a kairomone-based lure to recruit the predator for the biological control of T. absoluta and T. vaporariorum.

Survival of a specialist natural enemy experiencing resource competition with an omnivorous predator when sharing the invasive prey Tuta absoluta.

Can specialist natural enemies persist in ecosystems when competing with omnivorous natural enemies for their shared prey? The consequences of omnivory have been studied theoretically, but empirical studies are still lacking. Omnivory is nevertheless common in nature and omnivorous predators coexist with specialists in many ecosystems, even when they are intraguild predators. This type of association is also common in agroecosystems in which biological control strategies are used. Our study provides an example of the outcome of such an association in the context of biological control of the invasive pest Tuta absoluta (Lepidoptera) in a tomato agroecosystem. The two natural enemies involved, that is, a specialist (Stenomesius japonicus (Hymenoptera) parasitoid) and an omnivore (Macrolophus pygmaeus (Hemiptera) predator), were able to coexist for 3 months in our experimental cages in the absence of metacommunity mechanisms (i.e., emigration and recolonization), contrary to theoretical expectations. However, they negatively affected each other's population dynamics. We found that spatial resource segregation was not a mechanism that promoted their coexistence. Regarding pest control, the specialist and omnivorous natural enemies were found to exhibit complementary functional traits, leading to the best control when together. Mechanisms that may have promoted the coexistence of the two species as well as consequences with regard to the inoculative biological control program are discussed.

New parasitoid-predator associations: female parasitoids do not avoid competition with generalist predators when sharing invasive prey.

Optimal habitat selection is essential for species survival in ecosystems, and interspecific competition is a key ecological mechanism for many observed species association patterns. Specialized animal species are commonly affected by resource and interference competition with generalist and/or omnivorous competitors, so avoidance behavior could be expected. We hypothesize that specialist species may exploit broad range cues from such potential resource competitors (i.e., cues possibly common to various generalist and/or omnivorous predators) to avoid costly competition regarding food or reproduction, even in new species associations. We tested this hypothesis by studying short-term interactions between a native larval parasitoid and a native generalist omnivorous predator recently sharing the same invasive host/prey, the leaf miner Tuta absoluta. We observed a strong negative effect of kleptoparasitism (food resource stealing) instead of classical intraguild predation on immature parasitoids. There was no evidence that parasitoid females avoided the omnivorous predator when searching for oviposition sites, although we studied both long- and short-range known detection mechanisms. Therefore, we conclude that broad range cue avoidance may not exist in our biological system, probably because it would lead to too much oviposition site avoidance which would not be an efficient and, thus, beneficial strategy. If confirmed in other parasitoids or specialist predators, our findings may have implications for population dynamics, especially in the current context of increasing invasive species and the resulting creation of many new species associations.

Natural enemy-mediated indirect interactions among prey species: potential for enhancing biocontrol services in agroecosystems.

Understanding how arthropod pests and their natural enemies interact in complex agroecosystems is essential for pest management programmes. Theory predicts that prey sharing a predator, such as a biological control agent, can indirectly reduce each other's density at equilibrium (apparent competition). From this premise, we (i) discuss the complexity of indirect interactions among pests in agroecosystems and highlight the importance of natural enemy-mediated indirect interactions other than apparent competition, (ii) outline factors that affect the nature of enemy-mediated indirect interactions in the field and (iii) identify the way to manipulate enemy-mediated interactions for biological control. We argue that there is a need to increase the link between community ecology theory and biological control to develop better agroecological methods of crop protection via conservation biological control. In conclusion, we identify (i) interventions to be chosen depending on agroecosystem characteristics and (ii) several lines of research that will improve the potential for enemy-mediated indirect interactions to be applied to biological control.

Suitability of the pest-plant system Tuta absoluta (Lepidoptera: Gelechiidae)-tomato for Trichogramma (Hymenoptera: Trichogrammatidae) parasitoids and insights for biological control.

The South American tomato leafminer, Tuta absoluta Meyrick (Lepidoptera: Gelechiidae), is a major pest that has recently invaded Afro-Eurasia. Biological control, especially by Trichogramma parasitoids, is considered to be promising as a management tool for this pest. However, further development of Trichogramma-based biocontrol strategies would benefit from assessing the impact of released parasitoid offspring on the pest. Under laboratory conditions, we 1) compared the parasitism of five Trichogramma species-strains on the pest-plant system T. absoluta-tomato, and 2) assessed various biological traits of parasitoids, mass-reared on a factitious host (Ephestia kuehniella Zeller), when developing on T. absoluta. In addition, we evaluated the overall efficiency of two specific Trichogramma species when released under greenhouse conditions in combination with a common natural enemy in tomato crop, the predator Macrolophus pygmaeus Rambur. Parasitoids emerging from T. absoluta on tomato showed lower parasitism rates and poor biological traits, for example, wing deformations, reduced longevity, when compared with the control reared on the factitious host. Under greenhouse conditions, the parasitoids that developed on T. absoluta after initial releases contributed little to biological control of T. absoluta, and parasitism tended to be lower when the predator was present. However, a slightly higher T. absoluta control level was achieved by combining the predator and release of the parasitoid Trichogramma achaeae Nagaraja and Nagarkatti. This study shows that Trichogramma parasitoids may not build up populations on the T. absoluta-tomato system, but that Trichogramma parasitoids can be used in combination with M. pygmaeus to enhance biological control of the pest in tomato crops.

Assessing European egg parasitoids as a mean of controlling the invasive South American tomato pinworm Tuta absoluta.

The South American tomato pinworm (Tuta absoluta) has recently invaded Europe and is rapidly spreading in the Afro-Eurasian continent where it is becoming a major pest on tomato crops. Laboratory tests were undertaken to evaluate the potential of 29 European strains of Trichogramma parasitoids to control T. absoluta. In addition to the host itself, the host plant (tomato) was used during the laboratory tests in order to increase the chance of selecting the best parasitoid strains. Trichogramma females were placed with T. absoluta eggs on a tomato leaflet in tubes. We compared the parasitism of T. absoluta by the various Trichogramma species tested to the Trichogramma species currently commercially available for the pest control in Europe, i.e. Trichogramma achaeae. Thereafter, the more promising strains were tested on a larger scale, in mesocosm (i.e. cages in greenhouses) and in greenhouse compartments to evaluate efficiency of laboratory selected strains under cropping conditions. The most efficient strain from the laboratory screening trials did not perform as efficiently under the greenhouse conditions. We discuss differences in parasitism levels among species and strains and among the different scales tested in the experiments, as well as implications of these results for further screening for biocontrol agents.