Bottom-Up Forces in Agroecosystems and Their Potential Impact on Arthropod Pest Management.

Bottom-up effects are major ecological forces in crop-arthropod pest-natural enemy multitrophic interactions. Over the past two decades, bottom-up effects have been considered key levers for optimizing integrated pest management (IPM). Irrigation, fertilization, crop resistance, habitat manipulation, organic management practices, and landscape characteristics have all been shown to trigger marked bottom-up effects and thus impact pest management. In this review, we summarize current knowledge on the role of bottom-up effects in pest management and the associated mechanisms, and discuss several key study cases showing how bottom-up effects practically promote natural pest control. Bottom-up effects on IPM also contribute to sustainable intensification of agriculture in the context of agricultural transition and climate change. Finally, we highlight new research priorities in this important area. Together with top-down forces (biological control), future advances in understanding ecological mechanisms underlying key bottom-up forces could pave the way for developing novel pest management strategies and new optimized IPM programs.

Feeding guild determines strength of top-down forces in multitrophic system experiencing bottom-up constraints.

Nitrogen (N) and water are crucial in crop production but increasingly scarce environmental resources. Reducing their inputs can affect the whole plant-arthropod community including biocontrol agents. In a multitrophic system, we studied the interaction of the bottom-up effects of moderately reduced N concentration and/or water supply as well as the top-down effects of pests of different feeding guilds on plant nutritional quality (N and carbon concentration), direct defense (alkaloids and phenolics), and indirect defense (plant volatile organic compounds); on herbivore performance and host quality (N and carbon) to parasitoids and the latter's performance. Studied organisms were tomato plants, the sap feeders Macrosiphum euphorbiae and Bemisia tabaci, the leaf chewers Tuta absoluta and Spodoptera littoralis, and the parasitic wasps Aphelinus abdominalis and Necremnus tutae. Resource limitation affected plant quality, triggering bottom-up effects on herbivore and parasitoid performance, except for T. absoluta and N. tutae. Feeding guild had a major influence: bottom-up effects were stronger on sap feeders; N effects were stronger on sap feeders while water effects were stronger with leaf chewers (S. littoralis). Top-down effects of leaf chewer herbivory partly attenuated bottom-up effects and partly suppressed plant defenses. Bottom-up effects weakened when cascading up trophic levels. In summary, the interaction between plants, pests, and beneficial insects was modulated by abiotic factors, affecting insect performance. Simultaneous abiotic and biotic impact shaped plant biochemistry depending on the feeding guild: the biotic top-down effect of leaf chewer herbivory attenuated the bottom-up effects of plant nutrition and hence dominated the plant biochemical profile whereas in sap feeder infested leaves, it corresponded to the abiotic impact. This study highlights the plant's finely tuned regulatory system facilitating response prioritization. It offers perspectives on how smart manipulation of plant nutrient solutions might save resources while maintaining efficient biocontrol in crop production.

Untargeted metabolomic and molecular network approaches to reveal tomato root secondary metabolites.

INTRODUCTION: The tomato plant, Solanum lycopersicum L. (Solanaceae), is one of the most widely consumed vegetables in the world and plays an important role in human diet. Tomato cultivars are hosts for diverse types of pests, implying diverse chemical defence strategies. Glycoalkaloids are the main specialised metabolites produced by tomato leaves and fruits to protect against pests. However, the roots have received little attention, leading to limited knowledge about their phytochemical content. OBJECTIVE: The main goal of the current study was the development of an untargeted ultra-high-performance liquid chromatography high-resolution mass spectrometry (UHPLC-HRMS) based metabolomic approach to study phytochemical variations in tomato roots at two different development stages (i.e. 34th and 62nd day after sowing). METHODS: UHPLC-HRMS was used to establish the fingerprint of 24 batches of tomato roots. Statistical analyses were performed to highlight the compounds that discriminated between young and mature tomato roots. A dereplication strategy using molecular networking and HRMS/MS data was set up to identify the metabolites regulated during early root development. KEY FINDINGS: The main biomarkers were guanidine and adenosine derivatives associated with tryptophan. Secondary metabolites such as glycoalkaloids and steroidal alkaloids were also characterised. Most of the metabolites were up-regulated in young tomato roots (34 days old) while tryptophan was up-regulated in the older roots (62 days old). CONCLUSION: The metabolic changes observed in this work contribute to a deeper understanding of early-stage root development and may help our understanding of the complex processes involved in the tomato root defence arsenal.

Sublethal effects of beta-cypermethrin modulate interspecific interactions between specialist and generalist aphid species on soybean.

In agroecosystems, plant-pest interactions are at the basis of complex food webs, which can be affected by both biotic and abiotic factors. In the present study, we evaluated the impact of the insecticide beta-cypermethrin on interspecific interactions between the specialist aphid Aphis glycines and the generalist aphid Aulacorthum solani on soybean. Aphis glycines showed higher fecundity than A. solani on soybean and the aphids caused unbalanced reduction in population growth on each other. A sublethal concentration of beta-cypermethrin (LC5 for A. glycines) stimulated the reproduction of A. glycines but it did not impact the fecundity of A. solani. However, the LC5 of beta-cypermethrin enhanced the interspecific inhibition of fecundity between the two aphid species. Moreover, the two species showed different spatial distribution on soybean seedlings. Aphis glycines mainly aggregated on the stem of soybean plant while A. solani colonized soybean leaves. The LC5 of beta-cypermethrin drove A. solani migrating from soybean leaves to stems independently of interspecific competition. Aphis glycines facilitated A. solani colonization on soybean plant through impacting host susceptibility, and vice versa. Nevertheless, such facilitated colonization-induced susceptibility could be modulated through exposure to the LC5 of beta-cypermethrin. These findings hinted that the pyrethroid insecticide beta-cypermethrin has the potential to mediate the interspecific competition between specialist and generalist aphids (at the sublethal concentration of LC5), and that it could influence aphid population growth and community structure in soybean crops. This knowledge could contribute to rationalize application of insecticides and to optimize Integrated Pest Management in soybean.

Detrimental sublethal effects hamper the effective use of natural and chemical pesticides in combination with a key natural enemy of Bemisia tabaci on tomato.

BACKGROUND: Bemisia tabaci (Hemiptera: Aleyrodidae) represents one of the greatest threats to agricultural crops. Chemical control is the primary tool used in integrated pest management (IPM) programs. However, release of the predator Nesidiocoris tenuis (Hemiptera: Miridae) on tomato plants is a highly recommended control tactic. The objective of this study was to evaluate the efficacy of a commercial borax plus citrus oil (BCO) product against B. tabaci in the presence and absence of N. tenuis. The synthetic insecticide lambda-cyhalothrin was used as a positive control. We also evaluated the sublethal effects of BCO on the behavior and predation rate of N. tenuis. RESULTS: Our results demonstrated that BCO, alone and at its maximum recommended field rate for B. tabaci, was not effective in controlling the pest under laboratory conditions. Application of BCO simultaneous with N. tenuis release did not reduce the increase in the B. tabaci population. Effective control of B. tabaci was achieved using only N. tenuis. However, synthetic lambda-cyhalothrin pyrethroid, used here as a control, caused high pest mortality and led to on-site extinction of N. tenuis, which did not occur for insects exposed to BCO. Lambda-cyhalothrin and BCO significantly affected the foraging behavior of N. tenuis, reducing the predation rate, especially following exposure to lambda-cyhalothrin. CONCLUSION: The insecticide lambda-cyhalothrin achieved satisfactory results in suppressing B. tabaci, but was harmful to N. tenuis. Additionally, lambda-cyhalothrin and BCO affected predator behavior. © 2020 Society of Chemical Industry.

The preference-performance relationship as a means of classifying parasitoids according to their specialization degree.

Host range in parasitoids could be described by the preference-performance hypothesis (PPH) where preference is defined as host acceptance and performance is defined as the sum of all species on which parasitoid offspring can complete their life cycle. The PPH predicts that highly suitable hosts will be preferred by ovipositing females. However, generalist parasitoids may not conform to this hypothesis if they attack a large range of hosts of varying suitability. Under laboratory conditions, we tested the PPH relationship of three aphid parasitoids currently considered as generalist species (Aphelinus abdominalis, Aphidius ervi, Diaeretiella rapae). As expected, the three parasitoids species showed low selectivity, i.e., females stung all aphid species encountered (at least in some extent). However, depending on the parasitoid species, only 42%-58% of aphid species enabled producing parasitoid offspring. We did not find a correlation between the extent of preference and the performance of three generalist aphid parasitoids. For A. ervi, host phylogeny is also important as females showed higher attack and developmental rates on hosts closely related to the most suitable one. In addition, traits such as (a) the presence of protective secondary endosymbionts, for example, Hamiltonella defensa detected in Aphis fabae and Metopolophium dirhodum and (b) the sequestration of plant toxins as defense mechanism against parasitism, for example, in Aphis nerii and Brevicoryne brassicae, were likely at play to some extent in narrowing parasitoid host range. The lack of PPH relationship involved a low selectivity leading to a high adaptability, as well as selection pressure; the combination of which enabled the production of offspring in a new host species or a new environment. Testing for PPH relationships in parasitoids may provide useful cues to classify parasitoids in terms of specialization degree.

Global change-driven modulation of bottom-up forces and cascading effects on biocontrol services.

Abiotic and biotic factors affect plants in various ways which in turn affect associated arthropod communities through direct and/or indirect bottom-up interactions. Several review articles have synthesized studies examining the indirect effects of abiotic factors on plant-arthropod interactions, mainly focusing on soil nitrogen, soil water status, and climate change. However, these studies have mostly focused on bitrophic interactions, whereas most ecological systems are composed of at least three trophic levels. Lately, research on plant-mediated multitrophic interactions in plant-arthropod food web has received increasing interest. Both the intensification of agriculture and the global climate change have the potential to trigger bottom-up effects that cascade through trophic links. In this review article, we synthesize the most recent studies describing how abiotic changes could modulate plant-mediated bottom-up forces and how it could affect arthropod communities and associated biocontrol services. We discuss potential for increasing the sustainability of managed and natural ecosystems, and highlight road maps for future studies.

Nitrogen and water inputs to tomato plant do not trigger bottom-up effects on a leafminer parasitoid through host and non-host exposures.

BACKGROUND: Bottom-up and top-down forces are major components of biological control against pests in an agro-ecosystem. Understanding the multi-trophic interactions between plants and secondary consumers would help optimize pest control strategies. We manipulated nitrogen and/or water inputs to tomato plants (Solanum lycopersicum) to test whether these manipulations could trigger bottom-up effects on the parasitoid Necremnus tutae via host (Tuta absoluta) and/or non-host (Bemisia tabaci) exposures, and compared the control efficacy of N. tutae on T. absoluta in the presence and absence of B. tabaci. RESULTS: The results showed no cascading effects of plant nitrogen and/or water inputs on N. tutae via either host or non-host exposure. The bottom-up force was mitigated by chewing or sap-feeding insect consumers at the second energy level. By contrast, the top-down force on T. absoluta from parasitoids was enhanced by an additionally provided non-host, which could produce alternative food sources extending N. tutae longevity and enhancing the fitness of its offspring. CONCLUSION: Our results provided evidence for the combination of bottom-up and top-down approaches in tomato integrated pest management programs. © 2017 Society of Chemical Industry.

Does Plant Cultivar Difference Modify the Bottom-Up Effects of Resource Limitation on Plant-Insect Herbivore Interactions?

Variation in resource input to plants triggers bottom-up effects on plant-insect herbivore interactions. However, variation in plant intrinsic traits in response to resource availability may modify the bottom-up effects. Furthermore, the consequences also may depend on the feeding strategy of insect herbivores belonging to different feeding guilds. We evaluated the performance of two insect herbivores from distinct feeding guilds, the leaf miner Tuta absoluta and the phloem feeder Bemisia tabaci. We offered the insects two tomato cultivars growing under optimal nitrogen input vs. nitrogen limitation, or under optimal water input vs. water limitation. We found that: (i) the two cultivars differed in their responses to nitrogen and water limitation by regulating primary (leaf-gas exchange related parameters, leaf nitrogen content, and leaf C/N ratio) and secondary metabolism (main defensive compounds: glycoalkaloids); (ii) for both plant cultivars, nitrogen or water limitation significantly affected T. absoluta survival and development, while B. tabaci survival was affected only by nitrogen limitation; and surprisingly (iii) plant cultivar differences did not modify the negative bottom-up effects of resource limitation on the two insect herbivores. In conclusion, the negative effects of resource limitation cascaded up to insect herbivores even though plant cultivars exhibited various adaptive traits to resource limitation.

Increased water salinity applied to tomato plants accelerates the development of the leaf miner Tuta absoluta through bottom-up effects.

Variation in resource inputs to plants may trigger bottom-up effects on herbivorous insects. We examined the effects of water input: optimal water vs. limited water; water salinity: with vs. without addition of 100 mM NaCl; and their interactions on tomato plants (Solanum lycopersicum), and consequently, the bottom-up effects on the tomato leaf miner, Tuta absoluta (Meytick) (Lepidoptera: Gelechiidae). Plant growth was significantly impeded by limited water input and NaCl addition. In terms of leaf chemical defense, the production of tomatidine significantly increased with limited water and NaCl addition, and a similar but non-significant trend was observed for the other glycoalkaloids. Tuta absoluta survival did not vary with the water and salinity treatments, but the treatment "optimal water-high salinity" increased the development rate without lowering pupal mass. Our results suggest that caution should be used in the IPM program against T. absoluta when irrigating tomato crops with saline water.

Effect of plant nitrogen and water status on the foraging behavior and fitness of an omnivorous arthropod.

Omnivorous arthropods make dietary choices according to the environment in which they forage, mainly availability/quality of plant and/or prey resources. Such decisions and their subsequent impacts on life-history traits may be affected by the availability of nutrients and water to plants, that is, through bottom-up forces. By setting up arenas for feeding behavior observation as well as glasshouse cages for plant preference assessment, we studied effects of the presence of prey (Lepidoptera eggs) and nitrogen/water availability to host tomato plants on the foraging behavior and life-history traits in the omnivorous predator Macrolophus pygmaeus (Heteroptera: Miridae). In the absence of prey, the predator fed equally on the plants treated with various levels of nitrogen and water. In the presence of prey, however, the feeding rate on plants decreased when the plant received low water input. The feeding rate on prey was positively correlated with feeding rate on plants; that is, prey feeding increased with plant feeding when the plants received high water input. Moreover, plants receiving high water input attracted more M. pygmaeus adults compared with those receiving low water input. For M. pygmaeus fitness, the presence of prey enhanced its fertility and longevity, but the longevity decreased when plants received low compared with high water input. In conclusion, the omnivorous predator may be obliged to feed on plants to obtain water, and plant water status may be a limiting factor for the foraging behavior and fitness of the omnivorous predator.

Effects of Abiotic Factors on HIPV-Mediated Interactions between Plants and Parasitoids.

In contrast to constitutively emitted plant volatiles (PV), herbivore-induced plant volatiles (HIPV) are specifically emitted by plants when afflicted with herbivores. HIPV can be perceived by parasitoids and predators which parasitize or prey on the respective herbivores, including parasitic hymenoptera. HIPV act as signals and facilitate host/prey detection. They comprise a blend of compounds: main constituents are terpenoids and "green leaf volatiles." Constitutive emission of PV is well known to be influenced by abiotic factors like temperature, light intensity, water, and nutrient availability. HIPV share biosynthetic pathways with constitutively emitted PV and might therefore likewise be affected by abiotic conditions. However, the effects of abiotic factors on HIPV-mediated biotic interactions have received only limited attention to date. HIPV being influenced by the plant's growing conditions could have major implications for pest management. Quantitative and qualitative changes in HIPV blends may improve or impair biocontrol. Enhanced emission of HIPV may attract a larger number of natural enemies. Reduced emission rates or altered compositions, however, may render blends imperceptible to parasitoides and predators. Predicting the outcome of these changes is highly important for food production and for ecosystems affected by global climate change.

Nitrogen and water availability to tomato plants triggers bottom-up effects on the leafminer Tuta absoluta.

This study examined the effects of various levels of nitrogen inputs (optimal, insufficient and excessive) and water inputs (optimal, low drought and high drought) to tomato plants (Solanum lycopersicum) on survival and development of an invasive tomato leafminer, Tuta absoluta (Meytick) (Lepidoptera: Gelechiidae). Plant growth i.e. plant height and the number of nodes declined under insufficient or excessive nitrogen treatment. Compared to optimal N, insufficient N treatment decreased leaf N content and increased the carbon/nitrogen ratio (C/N) whereas an excess of N had no effect on both leaf N content and leaf C/N ratio. Sub-optimal nitrogen supplies, water treatments and their interactions, significantly reduced the leafminer survival rate and slowed down its development. Together with the findings from three recent companion studies, we assumed that a combination of changes in nutritional value and chemical defense could explain these observed effects. Furthermore, our findings supported both the "Plant vigor hypothesis" and the "Nitrogen limitation hypothesis".

Direct and indirect impact of sewage sludge compost spreading on Quercus coccifera monoterpene emissions in a Mediterranean shrubland.

Monoterpene emissions of Quercus coccifera L. were repeatedly measured during the two years following the spreading of a sewage sludge compost at rates of 50 Mg ha⁻¹ and 100 Mg ha⁻¹, in a twelve-year-old post-fire Mediterranean shrubland. We also monitored the patterns of change in soil and leaf nutrient content, plant water potential, chlorophyll fluorescence, and plant growth. Compost spreading resulted in weak changes in leaf nutrient content and plant water status, and therefore no significant effect on monoterpene emissions at leaf scale, except during one summer sampling, probably related to advanced leaf maturity with the highest compost rate. However, compost increased plant growth, particularly the leaf biomass. The results suggest that compost spreading in Mediterranean shrublands has no strong short-term effect on Q. coccifera monoterpene emissions at leaf level, but may indirectly increase volatile organic compound fluxes at the stand scale, which may contribute to regional ozone pollution.

Do photosynthetic limitations of evergreen Quercus ilex leaves change with long-term increased drought severity?

Seasonal drought can severely impact leaf photosynthetic capacity. This is particularly important for Mediterranean forests, where precipitation is expected to decrease as a consequence of climate change. Impacts of increased drought on the photosynthetic capacity of the evergreen Quercus ilex were studied for two years in a mature forest submitted to long-term throughfall exclusion. Gas exchange and chlorophyll fluorescence were measured on two successive leaf cohorts in a control and a dry plot. Exclusion significantly reduced leaf water potential in the dry treatment. In both treatments, light-saturated net assimilation rate (A(max)), stomatal conductance (g(s)), maximum carboxylation rate (V(cmax)), maximum rate of electron transport (J(max)), mesophyll conductance to CO2 (g(m)) and nitrogen investment in photosynthesis decreased markedly with soil water limitation during summer. The relationships between leaf photosynthetic parameters and leaf water potential remained identical in the two treatments. Leaf and canopy acclimation to progressive, long-term drought occurred through changes in leaf area index, leaf mass per area and leaf chemical composition, but not through modifications of physiological parameters.

Modelling the drought impact on monoterpene fluxes from an evergreen Mediterranean forest canopy.

In many ecosystems drought cycles are common during the growing season but their impact on volatile monoterpene emissions is unclear. Therefore, we aimed to develop and evaluate a process-based modelling approach to explore the explanatory power of likely mechanisms. The biochemically based isoprene and monoterpene emission model SIM-BIM2 has been modified and linked to a canopy model and a soil water balance model. Simulations are carried out for Quercus ilex forest sites and results are compared to measured soil water, photosynthesis, terpene-synthase activity, and monoterpene emission rates. Finally, the coupled model system is used to estimate the annual drought impact on photosynthesis and emission. The combined and adjusted vegetation model was able to simulate photosynthesis and monoterpene emission under dry and irrigated conditions with an R(2) of 0.74 and 0.52, respectively. We estimated an annual reduction of monoterpene emission of 67% for the extended and severe drought period in 2006 in the investigated Mediterranean ecosystem. It is concluded that process-based ecosystem models can provide a useful tool to investigate the involved mechanisms and to quantify the importance of specific environmental constraints.