Overcompensation of herbivore reproduction through hyper-suppression of plant defenses in response to competition.

Spider mites are destructive arthropod pests on many crops. The generalist herbivorous mite Tetranychus urticae induces defenses in tomato (Solanum lycopersicum) and this constrains its fitness. By contrast, the Solanaceae-specialist Tetranychus evansi maintains a high reproductive performance by suppressing tomato defenses. Tetranychus evansi outcompetes T. urticae when infesting the same plant, but it is unknown whether this is facilitated by the defenses of the plant. We assessed the extent to which a secondary infestation by a competitor affects local plant defense responses (phytohormones and defense genes), mite gene expression and mite performance. We observed that T. evansi switches to hyper-suppression of defenses after its tomato host is also invaded by its natural competitor T. urticae. Jasmonate (JA) and salicylate (SA) defenses were suppressed more strongly, albeit only locally at the feeding site of T. evansi, upon introduction of T. urticae to the infested leaflet. The hyper-suppression of defenses coincided with increased expression of T. evansi genes coding for salivary defense-suppressing effector proteins and was paralleled by an increased reproductive performance. Together, these observations suggest that T. evansi overcompensates its reproduction through hyper-suppression of plant defenses in response to nearby competitors. We hypothesize that the competitor-induced overcompensation promotes competitive population growth of T. evansi on tomato.

Nematode Root Herbivory in Tomato Increases Leaf Defenses and Reduces Leaf Miner Oviposition and Performance.

The outcome of plant-mediated interactions among herbivores from several feeding guilds has been studied intensively. However, our understanding on the effects of nematode root herbivory on leaf miner oviposition behavior and performance remain limited. In this study, we evaluated whether Meloidogyne incognita root herbivory affects Tuta absoluta oviposition preference on Solanum lycopersicum plants and the development of the resulting offspring. To investigate the M. incognita-herbivory induced plant systemic responses that might explain the observed biological effects, we measured photosynthetic rates, leaf trypsin protease inhibitor activities, and analyzed the profile of volatiles emitted by the leaves of root-infested and non-infested plants. We found that T. absoluta females avoided laying eggs on the leaves of root-infested plants, and that root infestation negatively affected the pupation process of T. absoluta. These effects were accompanied by a strong suppression of leaf volatile emissions, a decrease in photosynthetic rates, and an increase in the activity of leaf trypsin protease inhibitors. Our study reveals that root attack by nematodes can shape leaf physiology, and thereby increases plant resistance.

Spider mites suppress tomato defenses downstream of jasmonate and salicylate independently of hormonal crosstalk.

Plants respond to herbivory by mounting a defense. Some plant-eating spider mites (Tetranychus spp.) have adapted to plant defenses to maintain a high reproductive performance. From natural populations we selected three spider mite strains from two species, Tetranychus urticae and Tetranychus evansi, that can suppress plant defenses, using a fourth defense-inducing strain as a benchmark, to assess to which extent these strains suppress defenses differently. We characterized timing and magnitude of phytohormone accumulation and defense-gene expression, and determined if mites that cannot suppress defenses benefit from sharing a leaf with suppressors. The nonsuppressor strain induced a mixture of jasmonate- (JA) and salicylate (SA)-dependent defenses. Induced defense genes separated into three groups: 'early' (expression peak at 1 d postinfestation (dpi)); 'intermediate' (4 dpi); and 'late', whose expression increased until the leaf died. The T. evansi strains suppressed genes from all three groups, but the T. urticae strain only suppressed the late ones. Suppression occurred downstream of JA and SA accumulation, independently of the JA-SA antagonism, and was powerful enough to boost the reproductive performance of nonsuppressors up to 45%. Our results show that suppressing defenses not only brings benefits but, within herbivore communities, can also generate a considerable ecological cost when promoting the population growth of a competitor.

Efficacy of Conventional and Biorational Insecticides against the Invasive Pest Thrips parvispinus (Thysanoptera: Thripidae) under Containment Conditions.

In 2020, the invasive Thrips parvispinus (Karny) was first detected in Florida, United States. In response to the implemented regulatory restrictions, we conducted laboratory experiments under containment conditions. Thrips larvae and adults were exposed to 32 products (conventional and biorational insecticides) either directly or indirectly. Direct exposure was performed using a Spray Potter Tower, while indirect exposure was conducted by evaluating residue toxicity against the thrips. Water served as a control. We assessed mortality and leaf-feeding damage 48 h post-treatment. Among the conventional insecticides, chlorfenapyr, sulfoxaflor-spinetoram, and spinosad caused high mortality across all stages in both direct and residue toxicity assays. Pyridalyl, acetamiprid, tolfenpyrad, cyclaniliprole-flonicamid, acephate, novaluron, abamectin, cyantraniliprole, imidacloprid, cyclaniliprole, spirotetramat, and carbaryl displayed moderate toxicity, affecting at least two stages in either exposure route. Additionally, chlorfenapyr, spinosad, sulfoxaflor-spinetoram, pyridalyl, acetamiprid, cyclaniliprole, cyclaniliprole-flonicamid, abamectin, and acephate inhibited larvae and adult's leaf-feeding damage in both direct and residue toxicity assays. Regarding biorational insecticides, mineral oil (3%) and sesame oil caused the highest mortality and lowest leaf-feeding damage. Greenhouse evaluations of spinosad, chlorfenapyr, sulfoxaflor-spinetoram, and pyridalyl are recommended. Also, a rotation program incorporating these products, while considering different modes of action, is advised for ornamental growers to avoid resistance and to comply with regulations.

Exploring market-available pheromone lures and traps for monitoring Anthonomus testaceosquamosus (Coleoptera: Curculionidae).

The hibiscus bud weevil (HBW), Anthonomus testaceosquamosus Linell (Coleoptera: Curculionidae), is a significant threat to tropical hibiscus (Hibiscus rosa-sinensis) in Florida, USA, since its invasion in 2017. As a regulated pest in the state, early detection is crucial. Based on the success of pheromone-based monitoring programs for other weevil pests, such as the boll weevil, cranberry weevil, and pepper weevil, this study explores the potential use of these pheromone lures for early detection of HBW. To account for differences in efficacy based on trap color, height, and design, different pheromone lure sizes (4 mm, 10 mm, full-size), trap types (Yellow sticky trap, Japanese beetle trap, Boll weevil trap), and heights (0 m, 1.1 m) were also tested in this study. In laboratory assays, males and females exhibited higher attraction to full-size cranberry weevil lure discs than other lure size-type combinations. In semi-field trials, yellow sticky traps baited with cranberry weevil lures captured more weevils than Japanese beetle or boll weevil traps baited with cranberry weevil lures, while trap height did not influence HBW capture. In semi-field, 4-choice bioassays, yellow sticky traps baited with cranberry weevil lures captured more HBW compared to yellow sticky traps baited with pepper weevil, boll weevil, or unbaited traps. Further research is required to thoroughly evaluate the cranberry weevil lure's efficacy in capturing HBW. Our study suggests the potential for utilizing yellow sticky traps baited with lures for early HBW detection and highlights the importance of selecting the appropriate lure, trap type, and height for optimal efficacy.

Volatile Characterization of Lychee Plant Tissues (Litchi chinensis) and the Effect of Key Compounds on the Behavior of the Lychee Erinose Mite (Aceria litchii).

Herbivore-Induced Plant Volatiles (HIPVs) are volatile signals emitted by plants to deter herbivores and attract their natural enemies. To date, it is unknown how lychee plants, Litchi chinensis, respond to the induction of leaf galls (erinea) caused by the lychee erinose mite (LEM), Aceria litchii. Aiming to reveal the role of HIPVs in this plant-mite interaction, we investigated changes in the volatile profile of lychee plants infested by LEM and their role on LEM preferences. The volatile profile of uninfested (flower buds, fruit, leaves and new leaf shoots) and infested plant tissue were characterized under different levels of LEM infestation. Volatiles were collected using head-space-solid phase microextraction (HS-SPME) followed by gas chromatography-mass spectrometry (GC-MS) analyses. Fifty-eight volatiles, including terpenoids, alcohols, aldehydes, alkanes, esters, and ketones classes were identified. Using dual-choice bioassays, we investigated the preference of LEM to uninfested plant tissues and to the six most abundant plant volatiles identified. Uninfested new leaf shoots were the most attractive plant tissues to LEM and LEM attraction or repellence to volatiles were mostly influenced by compound concentration. We discuss possible applications of our findings in agricultural settings.

Food decisions of an omnivorous thrips are independent from the indirect effects of jasmonate-inducible plant defences on prey quality.

Plant defensive substances can affect the quality of herbivores as prey for predators either directly or indirectly. Directly when the prey has become toxic since it ingested toxic plant material and indirectly when these defences have affected the size and/or nutritional value (both quality parameters) of prey or their abundance. To disentangle direct and indirect effects of JA-defences on prey quality for predators, we used larvae of the omnivorous thrips Frankliniella occidentalis because these are not directly affected by the jasmonate-(JA)-regulated defences of tomato. We offered these thrips larvae the eggs of spider mites (Tetranychus urticae or T. evansi) that had been feeding from either normal tomato plants, JA-impaired plants, or plants treated with JA to artificially boost defences and assessed their performance. Thrips development and survival was reduced on the diet of T. evansi eggs relative to the diet of T. urticae eggs yet these effects were independent from the absence/presence of JA-defences. This indicates that the detrimental effects of tomato JA-defences on herbivores not necessarily also affects their quality as prey.

Spatiotemporal heterogeneity of tomato induced defense responses affects spider mite performance and behavior.

When feeding from tomato (Solanum lycopersicum), the generalist spider mite Tetranychus urticae induces jasmonate (JA)- and salicylate (SA)-regulated defense responses that hamper its performance. The related T. evansi, a Solanaceae-specialist, suppresses these defenses, thereby upholding a high performance. On a shared leaf, T. urticae can be facilitated by T. evansi, likely via suppression of defenses by the latter. Yet, when infesting the same plant, T. evansi outcompetes T. urticae. Recently, we found that T. evansi intensifies suppression of defenses locally, i.e., at its feeding site, after T. urticae mites were introduced onto adjacent leaf tissue. This hyper-suppression is paralleled by an increased oviposition rate of T. evansi, probably promoting its competitive population growth. Here we present additional data that not only provide insight into the spatiotemporal dynamics of defense induction and suppression by mites, but that also suggest T. evansi to manipulate more than JA and SA defenses alone.

Induced plant-defenses suppress herbivore reproduction but also constrain predation of their offspring.

Inducible anti-herbivore defenses in plants are predominantly regulated by jasmonic acid (JA). On tomato plants, most genotypes of the herbivorous generalist spider mite Tetranychus urticae induce JA defenses and perform poorly on it, whereas the Solanaceae specialist Tetranychus evansi, who suppresses JA defenses, performs well on it. We asked to which extent these spider mites and the predatory mite Phytoseiulus longipes preying on these spider mites eggs are affected by induced JA-defenses. By artificially inducing the JA-response of the tomato JA-biosynthesis mutant def-1 using exogenous JA and isoleucine (Ile), we first established the relationship between endogenous JA-Ile-levels and the reproductive performance of spider mites. For both mite species we observed that they produced more eggs when levels of JA-Ile were low. Subsequently, we allowed predatory mites to prey on spider mite-eggs derived from wild-type tomato plants, def-1 and JA-Ile-treated def-1 and observed that they preferred, and consumed more, eggs produced on tomato plants with weak JA defenses. However, predatory mite oviposition was similar across treatments. Our results show that induced JA-responses negatively affect spider mite performance, but positively affect the survival of their offspring by constraining egg-predation.