Changes in plant responses induced by an arthropod influence the colonization behavior of a subsequent herbivore.

BACKGROUND: Plants in nature can be sequentially attacked by different arthropod herbivores. Feeding by one arthropod species may induce plant-defense responses that might affect the performance of a later-arriving herbivorous species. Understanding these interactions can help in developing pest-management strategies. In tomato, the sweet-potato whitefly Bemisia tabaci and the two-spotted spider mite Tetranychus urticae are key pests that frequently cohabit on the same plant. We studied whether colonization by one species can either facilitate or impede later colonization of tomato plants by conspecific or heterospecific individuals. RESULTS: B. tabaci females showed a strong preference for and increased oviposition on plants previously colonized by conspecifics. In contrast, plants infested with T. urticae repelled B. tabaci females and reduced their oviposition rate by 86%. Although females of T. urticae showed no preference between conspecific-infested or uninfested plants, we observed a 50% reduction in the number of eggs laid on conspecific-infested plants. Both herbivorous arthropods up-regulated the expression of genes involving the jasmonic acid and abscisic acid pathways, increasing emissions of fatty-acid derivatives, but only B. tabaci increased the expression of genes related to the salicylic acid pathway and the total amount of phenylpropanoids released. Terpenoids were the most abundant compounds in the volatile blends; many terpenoids were emitted at different rates, which might have influenced the arthropods' host selection. CONCLUSION: Our results indicate that B. tabaci infestation facilitated subsequent infestations by conspecifics and mites, while T. urticae infestation promoted herbivore-induced resistance. Based on both the molecular and behavioral findings, a novel sustainable pest-management strategy is discussed.

Effects of Citrus Overwintering Predators, Host Plant Phenology and Environmental Variables on Aphid Infestation Dynamics in Clementine Citrus.

The Spirea citrus aphid, Aphis spiraecola Patch, and the cotton aphid, Aphis gossypii Glover (Hemiptera: Aphididae), are key pests of clementine mandarines in the Mediterranean basin. Severity of aphid infestations is determined by environmental variables, host plant phenology patterns, and the biological control exerted by their associated natural enemies. However, there is no information about the role these limiting and regulating factors play. Aphid densities, citrus phenology, and associated predators that overwinter in the crop were monitored weekly throughout two flush growth periods (February to July) in four clementine mandarin groves; relationships between these parameters and environmental variables (temperature and precipitation) were studied. Our results show exponential increase in aphid infestation levels to coincide with citrus phenological stages B3 and B4; shoots offer more space and nutritional resources for colony growth at these stages. Duration of these phenological stages, which was mediated by mean temperature, seems to importantly determine the severity of aphid infestations in the groves. Among those studied, the micro-coccinellids, mostly Scymnus species, were the only group of predators with the ability to efficiently regulate aphid populations. These natural enemies had the highest temporal and spatial demographic stability. Aphid regulation success was only achieved through early presence of natural enemies in the grove, at the aphid colonization phase. Our results suggest that conservation strategies aimed at preserving and enhancing Scymnus sp. populations may make an important contribution to the future success of the biological control of these key citrus pests.

Contribution of predation to the biological control of a key herbivorous pest in citrus agroecosystems.

Biological control has traditionally simplified the view of trophic relationships between herbivorous pests and their natural enemies in agriculture. The success or failure of this pest management strategy is still mainly attributed to the ability of a few key natural enemies to suppress the pest density. For example, successful regulation of the California red scale (Aonidiella aurantii), a key citrus pest, is generally credited to specific parasitoids of the Aphytis genus. Currently, research is revealing how herbivore regulation in agroecosystems can be alternatively achieved with a greater number of trophic associations within the system. The goals of the present study were as follows: i) to unravel species-specific trophic links between A. aurantii and its natural enemies in citrus agroecosystems, and ii) to assess their contribution to control of A. aurantii. Predation and parasitism of this herbivorous pest were assessed through exclusion experiments. Species-specific trophic links between this herbivorous pest and its natural enemies were studied using gut-content analysis of field-collected predators employing prey-specific DNA molecular markers. Relative predation rates of the species involved in A. aurantii regulation were estimated. Predation was found to be the main biotic component of A. aurantii mortality, causing reductions of more than 75% in recently settled cohorts. Aonidiella aurantii DNA was detected in the digestive system of 11 species of predators. Generalist and stenophagous predators, mainly associated with other citrus pests such as aphids, proved to be the most important biological control agents of this pest. Complex trophic relationships, such as apparent competition between two key citrus pests, were revealed. The present study highlights the role of predation as biotic mortality factor of key pests in perennial agroecosystems, wherein it is a rich complex of indigenous or naturalized generalist predators that are primarily responsible for this mortality. The results herein presented may therefore offer another perspective on the biological control of one of the key world-wide citrus pests, at least in those regions where specific parasitoids are not able to successfully regulate the scale populations.

Intraguild predation and competitive displacement between Nesidiocoris tenuis and Dicyphus maroccanus, two biological control agents in tomato pests.

Dicyphus maroccanus Wagner and Nesidiocoris tenuis Reuter (Hemiptera: Miridae) are 2 biological control agents in tomatoes. Through the crop seasons, a natural shift in the occurrence of both mirids in favor of N. tenuis has been observed at the end of the cropping cycle in eastern Spain. To better optimize their conservation, the reasons for the observed change, such as intraguild interactions (IGP) or the influence of environmental conditions, are worth elucidating. To do this, we first studied the IGP of adult females on heterospecific nymphs in the laboratory. We next studied exploitative competition between adults and nymphs of each species when feeding on Ephestia kueniella Zeller (Lepidoptera: Pyralidae) eggs in the laboratory. Finally, to analyze the competitive displacement between both mirids, we conducted a semifield experiment in which both predators were released together. All experiments were conducted at 2 temperature regimes (20 and 25°C). Adult-to-nymph intraguild interactions occurred only at 25 ºC at very low levels, showing that N. tenuis attacked and consumed a greater proportion of heterospecific nymphs. Nesidiocoris tenuis was a better competitor than D. maroccanus when feeding on the shared prey in the presence of its heterospecific nymph at 25 ºC. In semifield conditions, N. tenuis showed a competitive advantage over D. maroccanus at both temperatures. We conclude that there is not direct interference between both species, however, N. tenuis has a greater ability to outcompete, since it is best adapted to higher temperatures and it is able to remove food sources for D. maroccanus.