The presence of multiple parasitoids decreases host survival under warming, but parasitoid performance also decreases.

Current global changes are reshaping ecological communities and modifying environmental conditions. We need to recognize the combined impact of these biotic and abiotic factors on species interactions, community dynamics and ecosystem functioning. Specifically, the strength of predator-prey interactions often depends on the presence of other natural enemies: it weakens with competition and interference or strengthens with facilitation. Such effects of multiple predators on prey are likely to be affected by changes in the abiotic environment, altering top-down control, a key structuring force in natural and agricultural ecosystems. Here, we investigated how warming alters the effects of multiple predators on prey suppression using a dynamic model coupled with empirical laboratory experiments with Drosophila-parasitoid communities. While multiple parasitoids enhanced top-down control under warming, parasitoid performance generally declined when another parasitoid was present owing to competitive interactions. This could reduce top-down control over multiple generations. Our study highlights the importance of accounting for interactive effects between abiotic and biotic factors to better predict community dynamics in a rapidly changing world and thus better preserve ecosystem functioning and services such as biological control.

Multiple parasitoid species enhance top-down control, but parasitoid performance is context dependent.

Ecological communities are composed of many species, forming complex networks of interactions. Current environmental changes are altering the structure and species composition of ecological networks, which could modify interactions, either directly or indirectly. To predict changes in the functioning of communities, we need to understand whether species interactions are primarily driven by network structure (i.e. topology) or the specific identities of species (i.e. nodes). Yet, this partitioning of effects is challenging and thus rarely explored. Here we disentangled the influence of network structure and the identities of species on the outcome of consumer-resource interactions using a host-parasitoid system. We used four common community modules in host-parasitoid communities to represent network structure (i.e. host-parasitoid, exploitative competition, alternative host and a combination of exploitative competition and alternative host). We assembled nine different species combinations per community module in a laboratory experiment using a pool of three Drosophila hosts and three larval parasitoid species (Leptopilina sp., Ganaspis sp. and Asobara sp.). We compared host suppression and parasitoid performance across community modules and species assemblages to identify general effects linked to network structure and specific effects due to species community composition. We found that multiple parasitoid species enhanced host suppression due to sampling effect, weaker interspecific than intraspecific competition between parasitoids, and synergism. However, the effects of network structure on parasitoid performance were species specific and dependent on the identity of co-occurring species. Consequently, multiple parasitoid species generally strengthen top-down control, but the performance of the parasitoids depends on the identity of either the co-occurring parasitoid species, the alternative host species or both. Our results highlight the importance of preserving parasitoid diversity for ecosystem functioning and show that other effects depend on species community composition, and may therefore be altered by ongoing environmental changes.

Drought stress promotes the colonization success of a herbivorous mite that manipulates plant defenses.

Climate change is expected to bring longer periods of drought and this may affect the plant's ability to resist pests. We assessed if water deficit affects the tomato russet mite (TRM; Aculops lycopersici), a key tomato-pest. TRM thrives on tomato by suppressing the plant's jamonate defenses while these defenses typically are modulated by drought stress. We observed that the TRM population grows faster and causes more damage on drought-stressed plants. To explain this observation we measured several nutrients, phytohormones, defense-gene expression and the activity of defensive proteins in plants with or without drought stress or TRM. TRM increased the levels of total protein and several free amino acids. It also promoted the SA-response and upregulated the accumulation of jasmonates but down-regulated the downstream marker genes while promoting the activity of cysteine-but not serine-protease inhibitors, polyphenol oxidase and of peroxidase (POD). Drought stress, in turn, retained the down regulation of JA-marker genes and reduced the activity of serine protease inhibitors and POD, and altered the levels of some free-amino acids. When combined, drought stress antagonized the accumulation of POD and JA by TRM and synergized accumulation of free sugars and SA. Our data show that drought stress interacts with pest-induced primary and secondary metabolic changes and promotes pest performance.

Early Molecular Responses of Tomato to Combined Moderate Water Stress and Tomato Red Spider Mite Tetranychus evansi Attack.

Interaction between plants and their environment is changing as a consequence of the climate change and global warming, increasing the performance and dispersal of some pest species which become invasive species. Tetranychus evansi also known as the tomato red spider mite, is an invasive species which has been reported to increase its performance when feeding in the tomato cultivar Moneymaker (MM) under water deficit conditions. In order to clarify the underlying molecular events involved, we examined early plant molecular changes occurring on MM during T. evansi infestation alone or in combination with moderate drought stress. Hormonal profiling of MM plants showed an increase in abscisic acid (ABA) levels in drought-stressed plants while salicylic acid (SA) levels were higher in drought-stressed plants infested with T. evansi, indicating that SA is involved in the regulation of plant responses to this stress combination. Changes in the expression of ABA-dependent DREB2, NCED1, and RAB18 genes confirmed the presence of drought-dependent molecular responses in tomato plants and indicated that these responses could be modulated by the tomato red spider mite. Tomato metabolic profiling identified 42 differentially altered compounds produced by T. evansi attack, moderate drought stress, and/or their combination, reinforcing the idea of putative manipulation of tomato plant responses by tomato red spider mite. Altogether, these results indicate that the tomato red spider mite acts modulating plant responses to moderate drought stress by interfering with the ABA and SA hormonal responses, providing new insights into the early events occurring on plant biotic and abiotic stress interaction.

Plant-Mediated Effects of Water Deficit on the Performance of Tetranychus evansi on Tomato Drought-Adapted Accessions.

Climate change is expected to increase drought periods and the performance and dispersal of some invasive species such as Tetranychus evansi, which has been reported to take advantage of the nutritional changes induced by water-shortage on the tomato cultivar Moneymaker (MM). We have examined the implications for mite's biology of four accessions of the drought-adapted tomatoes, "Tomàtiga de Ramellet" (TR), under moderate drought stress. Mite performance was enhanced by drought in two accessions (TR61 and TR154), but not in the other two accessions (TR58 and TR126). We selected one accession of each outcome (i.e., TR154 and TR126) to further analyze plant nutritional parameters. We found that free sugars and most essential amino acids for mites were induced by drought and/or mite infestation on MM and TR154 plants, whereas sugars were not altered and a reduced number of essential amino acids were induced by drought in TR126. Remarkably, mite performance was enhanced by leaf infiltration of free sugars, essential amino acids mixture, and L-proline on well-watered MM and by free sugars on drought-stressed TR126 plants. These results indicate a positive link between the induction of soluble carbohydrates and amino acids used by the plant for osmotic adjustment and mite performance. The effects of drought and/or mite infestation on the defense response of plants was analyzed at three levels: phytohormone accumulation, the transcript levels of marker genes linked to jasmonates (JAs), salicylic acid (SA), and abscisic acid (ABA) pathways, and the activity of defense proteins. The ability of T. evansi to downregulate the accumulation of defense-related phytohormones was noted on MM and the two TR accessions analyzed (TR126 and TR154), though differences in the induction of protein defense genes and activities by drought and/or mite infestation were observed among them. These results emphasize the importance of studying plant biotic and abiotic stress factors in combination and provides an experimental framework for screening drought-tolerant tomato accessions that will be also resistant to herbivore mites.

Drought stress in tomato increases the performance of adapted and non-adapted strains of Tetranychus urticae.

The performance of the two-spotted spider mite, Tetranychus urticae Koch, on plants depends on the rate of adaptation of mite populations to each particular host and can be influenced by environmental conditions. We have tested the effects of drought stress, caused by water deficiency, in the interaction of tomato plants with tomato adapted (TA) and tomato non-adapted (TNA) strains of T. urticae. Our data revealed that mite performance was enhanced for the TA strain when reared on drought-stressed tomato plants, rising population growth and leaf damage. Population growth in the case of the TNA strain was negative, but they laid more eggs and the number of mobile forms was higher on drought-stressed tomato plants than on control plants. Water stress resulted in tomato plants with increased concentrations of essential amino acids and free sugars, improving the nutritional value of drought-stressed tomato plants for T. urticae. Mite infestation alone had almost no effect on the nutritional composition of tomato leaves, with the exception of an increase of free sugars. Tomato plant defense proteins were induced by both drought stress and mite infestation. However, the induction of protease inhibitors was higher in tomatoes exposed to mites from the TNA strain than in tomatoes that were fed upon by mites from the TA strain. The better performance of the TA strain could be associated to both changes in the digestive (cysteine and aspartyl protease and α-amylase activities) and detoxification (esterase activity) physiology of the mites and the attenuation of some of the plant defenses (protease inhibitors). Taken together, our results suggest that drought stress might favor outbreaks of T. urticae on tomato, by enhancing population growth of adapted populations and increasing the suitability of tomato as a host for non-adapted ones.

Drought-Stressed Tomato Plants Trigger Bottom-Up Effects on the Invasive Tetranychus evansi.

Climate change will bring more drought periods that will have an impact on the irrigation practices of some crops like tomato, from standard water regime to deficit irrigation. This will promote changes in plant metabolism and alter their interactions with biotic stressors. We have tested if mild or moderate drought-stressed tomato plants (simulating deficit irrigation) have an effect on the biological traits of the invasive tomato red spider mite, Tetranychus evansi. Our data reveal that T evansi caused more leaf damage to drought-stressed tomato plants (≥1.5 fold for both drought scenarios). Mite performance was also enhanced, as revealed by significant increases of eggs laid (≥2 fold) at 4 days post infestation (dpi), and of mobile forms (≥2 fold and 1.5 fold for moderate and mild drought, respectively) at 10 dpi. The levels of several essential amino acids (histidine, isoleucine, leucine, tyrosine, valine) and free sugars in tomato leaves were significantly induced by drought in combination with mites. The non-essential amino acid proline was also strongly induced, stimulating mite feeding and egg laying when added to tomato leaf disks at levels equivalent to that estimated on drought-infested tomato plants at 10 dpi. Tomato plant defense proteins were also affected by drought and/or mite infestation, but T. evansi was capable of circumventing their potential adverse effects. Altogether, our data indicate that significant increases of available free sugars and essential amino acids, jointly with their phagostimulant effect, created a favorable environment for a better T. evansi performance on drought-stressed tomato leaves. Thus, drought-stressed tomato plants, even at mild levels, may be more prone to T evansi outbreaks in a climate change scenario, which might negatively affect tomato production on area-wide scales.

Selection of Ceratitis capitata (Diptera: Tephritidae) specific recombinant monoclonal phage display antibodies for prey detection analysis.

Several recombinant antibodies against the Mediterranean fruit fly, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae), one of the most important pests in agriculture worldwide, were selected for the first time from a commercial phage display library of human scFv antibodies. The specificity and sensitivity of the selected recombinant antibodies were compared with that of a rabbit polyclonal serum raised in parallel using a wide range of arthropod species as controls. The selected recombinant monoclonal antibodies had a similar or greater specificity when compared with classical monoclonal antibodies. The selected recombinant antibodies were successfully used to detect the target antigen in the gut of predators and the scFv antibodies were sequenced and compared. These results demonstrate the potential for recombinant scFv antibodies to be used as an alternative to the classical monoclonal antibodies or even molecular probes in the post-mortem analysis studies of generalist predators.