Pollen provisioning attenuates pesticide side-effects on a phytoseiid predator.

BACKGROUND: Biological control with predatory mites is applied against pests in greenhouse crops. Chemical control with the use of selective, reduced-risk pesticides, is an important component of Integrated Pest Management (IPM) programs, that often needs to be combined with biological control. Here, we evaluated the effect of plant pollen when used as supplementary food on the survival, reproduction and predation of the predatory mite Amblydromalus limonicus (Acari: Phytoseiidae) after exposing young larvae and adults to flonicamid, an insecticide of moderate toxicity to phytoseiids. Pollen is an important alternative food for generalist phytoseiids ensuring survival and supporting populations build-up during periods of prey scarcity. Two regimes of cattail (Typha angustifolia L.) pollen differing in application frequency were used. In the first, the total amount of pollen was supplied once, within 30 min after insecticide application, whereas in the second regime, the same amount of pollen was supplied gradually, i.e., every 48 h. RESULTS: Regardless of the frequency of application, pollen provisioning results in a reduction in prey (thrips) consumption relative to the control (no pollen provisioning). Nevertheless, when adult mites were directly exposed to flonicamid residues, pollen provisioning attenuated the reduction in prey consumption as compared to the control. In addition, the gradual (every 48 h) provisioning of pollen to adult predators exposed to flonicamid residues impacted positively the intrinsic rate of population increase (rm) of A. limonicus as compared to when feeding on prey. CONCLUSION: Our results reveal an unexpected role of pollen provisioning in alleviating pesticides side-effects on phytoseiids. © 2024 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Plant-Mediated Effects of Beneficial Microbes and a Plant Strengthener against Spider Mites in Tomato.

The two-spotted spider mite Tetranychus urticae is a polyphagous herbivore with a worldwide distribution, and is a serious pest in tomato and other crops. As an alternative to chemical pesticides, biological control with the release of natural enemies such as predatory mites represent an efficient method to control T. urticae in many crops, but not in tomato. Other biological control agents, such as beneficial microbes, as well as chemical compounds, which can act as plant defense elicitors that confer plant resistance against pests and pathogens, may prove promising biological solutions for the suppression of spider mite populations in tomato. Here, we assessed this hypothesis by recording the effects of a series of fungal and bacterial strains and the plant strengthener acibenzolar-s-methyl for their plant-mediated effects on T. urticae performance in two tomato cultivars. We found significant negative effects on the survival, egg production and spider mite feeding damage on plants inoculated with microbes or treated with the plant strengthener as compared to the control plants. Our results highlight the potential of beneficial microbes and plant strengtheners in spider mite suppression in addition to plant disease control.

Predation efficiency of the green lacewings Chrysoperla agilis and C. mutata against aphids and mealybugs in sweet pepper.

Chrysoperla species include well-known predators of aphids and other soft-bodied arthropods. As such, they are considered important biological control agents of herbivorous pests in agroecosystems where many of green lacewings species occur. Despite the high number of species of the genus Chrysoperla, only a few have been assessed for the predation efficiency of their larvae against pests infesting plants, and even fewer are currently marketed for use in biocontrol practice. Difficulties in species identification within the Chrysoperla carnea complex species in particular has been related to varying success of commercial C. carnea s.l. releases in the field. In this study, we assessed the ability of two Chrysoperla species, Chrysoperla agilis a member of the carnea cryptic species group, and Chrysoperla mutata of the pudica group to consume aphid and mealybug individuals and suppress their populations in sweet pepper plants. We found that third-instar larvae of both species were able to consume a high number of aphids (approximately 120 nymphs per larva) and mealybugs (approximately 105 nymphs per larva) within 24 h. Furthermore, the release of second-instar larvae of both C. agilis and C. mutata was shown to be remarkably efficient in suppressing the pest populations in long-term greenhouse experiments. Aphid populations were suppressed by approximately 98% and mealybugs by 78% as compared to control plants. Our results highlight the predation efficiency and the biocontrol potential of two widespread Chrysoperla species for their use in pest control.

Effect of Duration of Exposure to Males on Female Reproductive Performance of the Green Lacewing, Chrysoperla agilis (Neuroptera: Chrysopidae).

Chrysoperla agilis Henry et al. is one of the five cryptic species of the carnea group found in Europe. They are known to widely occur in agricultural fields and survive and reproduce in a wide range of temperatures. The reproductive biology of the cryptic species is poorly known, especially regarding the number of matings required for the females' maximum reproductive output. We recorded the egg production and longevity of virgin females, as well as of females that had access to males for 1 week or for their lifetime. Longevity of C. agilis females with access to males was similar whether these were present for 1 week or for their lifetime (64.8 and 66.1 days, respectively). On the other hand, oviposition was higher in the long-term exposure to males (302.1 vs. 421.1 eggs, respectively). Virgin females lived longer (94.1 days) than mated females and laid a low number (54.5) of (unfertile) eggs. Egg hatchability and progeny sex ratio were similar in treatments with males. Nevertheless, the highest value (0.1321) of intrinsic rate of increase (rm) was recorded when females were continuously exposed to males. These results are relevant to biological control and could be applicable in mass-rearing C. agilis and predicting its population dynamics in the field.

Ménage à Trois: Unraveling the Mechanisms Regulating Plant-Microbe-Arthropod Interactions.

Plant-microbe-arthropod (PMA) three-way interactions have important implications for plant health. However, our poor understanding of the underlying regulatory mechanisms hampers their biotechnological applications. To this end, we searched for potential common patterns in plant responses regarding taxonomic groups or lifestyles. We found that most signaling modules regulating two-way interactions also operate in three-way interactions. Furthermore, the relative contribution of signaling modules to the final plant response cannot be directly inferred from two-way interactions. Moreover, our analyses show that three-way interactions often result in the activation of additional pathways, as well as in changes in the speed or intensity of defense activation. Thus, detailed, basic knowledge of plant-microbe-arthropod regulation will be essential for the design of environmentally friendly crop management strategies.

The Beneficial Endophytic Fungus Fusarium solani Strain K Alters Tomato Responses Against Spider Mites to the Benefit of the Plant.

Beneficial microorganisms are known to promote plant growth and confer resistance to biotic and abiotic stressors. Soil-borne beneficial microbes in particular have shown potential in protecting plants against pathogens and herbivores via the elicitation of plant responses. In this study, we evaluated the role of Fusarium solani strain K (FsK) in altering plant responses to the two spotted spider mite Tetranychus urticae in tomato. We found evidence that FsK, a beneficial endophytic fungal strain isolated from the roots of tomato plants grown on suppressive compost, affects both direct and indirect tomato defenses against spider mites. Defense-related genes were differentially expressed on FsK-colonized plants after spider mite infestation compared to clean or spider mite-infested un-colonized plants. In accordance, spider mite performance was negatively affected on FsK-colonized plants and feeding damage was lower on these compared to control plants. Notably, FsK-colonization led to increased plant biomass to both spider mite-infested and un-infested plants. FsK was shown to enhance indirect tomato defense as FsK-colonized plants attracted more predators than un-colonized plants. In accordance, headspace volatile analysis revealed significant differences between the volatiles emitted by FsK-colonized plants in response to attack by spider mites. Our results highlight the role of endophytic fungi in shaping plant-mite interactions and may offer the opportunity for the development of a novel tool for spider mite control.

Omnivore-herbivore interactions: thrips and whiteflies compete via the shared host plant.

Phytophagy is a common feature among pure herbivorous insects and omnivores that utilise both plant and prey as food resources; nevertheless, experimental evidence for factors affecting their interactions is restricted to intraguild predation and predator-mediated competition. We herein focused on plant-mediated effects that could result from plant defence activation or quality alteration and compared the performance of an omnivore, the western flower thrips Frankliniella occidentalis, and a pure herbivore, the greenhouse whitefly Trialeurodes vaporariorum, on cucumber plants previously infested with either species. Furthermore, we recorded their behavioural responses when given a choice among infested and clean plants. Whiteflies laid less eggs on plants previously exposed to thrips but more on whitefly-infested plants. Thrips survival was negatively affected on whitefly-infested than on thrips-infested or clean plants. Notably, whiteflies developed significantly faster on plants infested with conspecifics. In accordance, whiteflies avoided thrips-infested plants and preferred whitefly-infested over clean plants. Thrips showed no preference for either infested or clean plants. Our study is a first report on the role of plant-mediated effects in shaping omnivore-herbivore interactions. Considering the factors driving such interactions we will likely better understand the ecology of the more complex relationships among plants and pest organisms.

Induced plant defences in biological control of arthropod pests: a double-edged sword.

Biological control is an important ecosystem service delivered by natural enemies. Together with breeding for plant defence, it constitutes one of the most promising alternatives to pesticides for controlling herbivores in sustainable crop production. Especially induced plant defences may be promising targets in plant breeding for resistance against arthropod pests. Because they are activated upon herbivore damage, costs are only incurred when defence is needed. Moreover, they can be more specific than constitutive defences. Nevertheless, inducible defence traits that are harming plant pest organisms may interfere with biological control agents, such as predators and parasitoids. Despite the vast fundamental knowledge on plant defence mechanisms and their effects on natural enemies, our understanding of the feasibility of combining biological control with induced plant defence in practice is relatively poor. In this review, we focus on arthropod pest control and present the most important features of biological control with natural enemies and of induced plant defence. Furthermore, we show potential synergies and conflicts among them and, finally, identify gaps and list opportunities for their combined use in crop protection. We suggest that breeders should focus on inducible resistance traits that are compatible with the natural enemies of arthropod pests, specifically traits that help communities of natural enemies to build up. © 2017 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

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.

The role of phytophagy by predators in shaping plant interactions with their pests.

Zoophytophagy is common among predacious arthropods, but research on their role in plant-herbivore interactions is generally focused on predation effects whereas their phytophagy is largely neglected. Our recent study revealed the ability of zoophytophagous predators to induce defense related traits and to affect herbivore performance apart from predation through the plant. Additionally, we show here that predator-exposed plants suffer less damage compared to unexposed plants. Thus, zoophytophagous organisms likely shape community structure by both their predation on herbivores and their phytophagy. Here, we consider zoophytophagous predators as plant vaccination factors and outline how their dual role in affecting herbivores may impact their use in biological pest control. Because plant responses to phytophagy and phytopathogens are known to interact, zoophytophagous predators may also affect plant-pathogen interactions. When we consider these indirect interactions with different plant pest organisms, we will likely better understand the ecology of the complex relationships among plants, herbivores and predators. Moreover, a comprehensive knowledge on the effects of the phytophagy of predators in these ecological interactions will potentially allow us to enhance sustainability in pest control.

Beyond Predation: The Zoophytophagous Predator Macrolophus pygmaeus Induces Tomato Resistance against Spider Mites.

Many predatory insects that prey on herbivores also feed on the plant, but it is unknown whether plants affect the performance of herbivores by responding to this phytophagy with defence induction. We investigate whether the prior presence of the omnivorous predator Macrolophus pygmaeus (Rambur) on tomato plants affects plant resistance against two different herbivore species. Besides plant-mediated effects of M. pygmaeus on herbivore performance, we examined whether a plant defence trait that is known to be inducible by herbivory, proteinase inhibitors (PI), may also be activated in response to the interactions of this predator with the tomato plant. We show that exposing tomato plants to the omnivorous predator M. pygmaeus reduced performance of a subsequently infesting herbivore, the two-spotted spider mite Tetranychus urticae Koch, but not of the greenhouse whitefly Trialeurodes vaporariorum (Westwood). The spider-mite infested tomato plants experience a lower herbivore load, i.e., number of eggs deposited and individuals present, when previously exposed to the zoophytophagous predator. This effect is not restricted to the exposed leaf and persists on exposed plants for at least two weeks after the removal of the predators. The decreased performance of spider mites as a result of prior exposure of the plant to M. pygmaeus is accompanied by a locally and systemically increased accumulation of transcripts and activity of proteinase inhibitors that are known to be involved in plant defence. Our results demonstrate that zoophytophagous predators can induce plant defence responses and reduce herbivore performance. Hence, the suppression of populations of certain herbivores via consumption may be strengthened by the induction of plant defences by zoophytophagous predators.

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.

Compatibility of reduced-risk insecticides with the non-target predatory mite Iphiseius degenerans (Acari: Phytoseiidae).

BACKGROUND: Iphiseius degenerans (Berlese) (Acari: Phytoseiidae) is a common predatory mite in citrus orchards in some areas of the Mediterranean basin and an important biological control agent of the thrips Frankliniella occidentalis (Pergande) in Integrated Pest Management (IPM) programmes in greenhouse crops. In this study, we evaluated the effects of the 'reduced-risk' insecticides acetamiprid, chlorantraniliprole, flubendiamide, metaflumizone, methoxyfenozide, spinetoram and thiamethoxam on I. degenerans, as a means of testing their compatibility in IPM programmes. RESULTS: Although all pesticides decreased immature survival, high mortality was only recorded for young larvae when exposed to acetamiprid, while metaflumizone, thiamethoxam and spinetoram resulted in intermediate lethal effects. The estimated LC50 values of acetamiprid, spinetoram and thiamethoxam for I. degenerans females were 0.52, 0.84 and 0.16-fold lower than the respective maximum recommended doses of the pesticides for field application. Although all pesticides tested significantly decreased fecundity, highest rates corresponded to the three pesticides already mentioned. CONCLUSION: Chlorantraniliprole, flubendiamide and methoxyfenozide may preliminarily be included in IPM programmes, whereas the effects of acetamiprid, metaflumizone, spinetoram and thiamethoxam on I. degenerans should be clarified in further field toxicological tests. This information could be useful for rationally planning and implementing pest management on a sustainable basis.

Potential of the predatory mite Phytoseius finitimus (Acari: Phytoseiidae) to feed and reproduce on greenhouse pests.

Phytoseiid mites of the genus Phytoseius are natural enemies of tetranychid and eriophyid herbivorous mites mostly found on hairy plants where they feed on prey, as well as on pollen. Nevertheless, the nutritional ecology and the role of these predators in biological pest control are only rarely addressed. In the present study, we evaluated the potential of Phytoseius finitimus to feed and reproduce on three major greenhouse pests, the two-spotted spider mite, the greenhouse whitefly and the western flower thrips. Additionally, we estimated the effect of cattail pollen when provided to the predator alone or in mixed diets with prey. Contrary to thrips larvae, both spider mite larvae and whitefly crawlers sustained the development of P. finitimus. In addition, females consumed more spider mite eggs and larvae, as well as whitefly crawlers than thrips larvae, but laid eggs when feeding on all prey. When provided alone, cattail pollen sustained the development and reproduction of the predator. The addition of pollen in mixed diets with prey reduced prey consumption, though it increased the predator's egg production. We discuss the implications of our findings for biological pest control.

Effect of mating frequency on fecundity and longevity of the predatory mite Kampimodromus aberrans (Acari: Phytoseiidae).

The effect of single versus multiple mating on longevity and fecundity as well as the number of matings required to maximize a female's reproductive success of the predatory mite Kampimodromus aberrans Oudemans were studied under laboratory conditions. Newly emerged adult females of the stock colony of K. aberrans were placed individually on a bean leaf disc, and maintained at 25 degrees C and 16:8 LD. A young male remained with a female for limited periods or continuously. Mating was a requisite for oocyte maturation and oviposition. Females which mated three to four times during their life and females in continuous presence of males, laid significantly and considerably more eggs than single-mated females. Virgin females lived the longest, and those in continuous presence of males the shortest. In all cases and irrespective of the number of matings, the sex ratio of the offspring was male-biased in the first three to four days of oviposition period, and female-biased in later days.

Mating behavior of the predatory mite Kampimodromus aberrans (Acari: Phytoseiidae).

The mating behavior of the predatory mite Kampimodromus aberrans was studied in the laboratory at a constant temperature of 25 +/- 1 degrees C and a photoperiod of 16:8 (L:D). Forty pairs of newly emerged virgin females and unmated males, were maintained separately on leaf discs and their mating behavior, was observed continuously under a stereomicroscope. The mean time until first contact of female and male individuals was approximately 8.2 min. After the first contact the male moved to the top of the female's dorsum and subsequently underneath her in approximately 1.7 min and then the paired mites walked around on the leaf surface for approximately 7.5 min. Afterwards, the mites remained still in the mating position, i.e. the male beneath the female for an average period of 230.5 min. After mating, most of the females had one spermatophore in one of their spermathecae, whereas a few had one spermatophore in both spermathecae.