Archetype models upscale understanding of natural pest control response to land-use change.

Control of crop pests by shifting host plant availability and natural enemy activity at landscape scales has great potential to enhance the sustainability of agriculture. However, mainstreaming natural pest control requires improved understanding of how its benefits can be realized across a variety of agroecological contexts. Empirical studies suggest significant but highly variable responses of natural pest control to land-use change. Current ecological models are either too specific to provide insight across agroecosystems or too generic to guide management with actionable predictions. We suggest obtaining the full benefit of available empirical, theoretical, and methodological knowledge by combining trait-mediated understanding from correlative studies with the explicit representation of causal relationships achieved by mechanistic modeling. To link these frameworks, we adapt the concept of archetypes, or context-specific generalizations, from sustainability science. Similar responses of natural pest control to land-use gradients across cases that share key attributes, such as functional traits of focal organisms, indicate general processes that drive system behavior in a context-sensitive manner. Based on such observations of natural pest control, a systematic definition of archetypes can provide the basis for mechanistic models of intermediate generality that cover all major agroecosystems worldwide. Example applications demonstrate the potential for upscaling understanding and improving predictions of natural pest control, based on knowledge transfer and scientific synthesis. A broader application of this mechanistic archetype approach promises to enhance ecology's contribution to natural resource management across diverse regions and social-ecological contexts.

Interaction diversity explains the maintenance of phytochemical diversity.

The production of complex mixtures of secondary metabolites is a ubiquitous feature of plants. Several evolutionary hypotheses seek to explain how phytochemical diversity is maintained, including the synergy hypothesis, the interaction diversity hypothesis, and the screening hypothesis. We experimentally tested a set of predictions derived from these hypotheses by manipulating the richness and structural diversity of phenolic metabolites in the diets of eight plant consumers. Across 3940 total bioassays, there was clear support for the interaction diversity hypothesis over the synergy or screening hypotheses. The number of consumers affected by a particular phenolic composition increased with increasing richness and structural diversity of compounds. Furthermore, the bioactivity of phenolics was consumer-specific. All compounds tested reduced the performance of at least one consumer, but no compounds affected all consumers. These results show how phytochemical diversity may be maintained in nature by a complex selective landscape exerted by diverse communities of plant consumers.

Landscape composition mediates the relationship between predator body size and pest control.

Understanding the mechanisms contributing to positive relationships between predator diversity and natural pest control is fundamental to inform more effective management practices to support sustainable crop production. Predator body size can provide important insights to better understand and predict such predator-pest interactions. Yet, most studies exploring the link between predator body size and pest control have been conducted in species-poor communities under controlled environmental conditions, limiting our ability to generalize this relationship across heterogeneous landscapes. Using the community of naturally occurring ground beetles in cabbage fields, we examined how landscape composition (percent cropland) influences the size structure (mean, variance, and skewness of body size distribution) of predator communities and the subsequent effects on pest control. We found that predator communities shifted their size distribution toward larger body sizes in agriculturally dominated landscapes. This pattern arose from increasing numerical dominance of a few large-bodied species rather than an aggregated response across the community. Such landscape-driven changes in community size structure led to concomitant impacts on pest control, as the mean body size of predators was positively related to predation rates. Notably, the magnitude of pest control depended not only on the size of the dominant predators but was also strongly determined by the relative proportion of small vs. large-bodied species (i.e., skewness). Predation rates were higher in predator assemblages with even representation of small and large-bodied species relative to communities dominated by either large or small-bodied predators. Landscape composition may therefore modulate the relationship between predator body size and pest control by influencing the body size distribution of co-occurring species. Our study highlights the need to consider agricultural practices that not only boost effective predators, but also sustain a predator assemblage with a diverse set of traits to maximize overall pest control.

Crop pests and predators exhibit inconsistent responses to surrounding landscape composition.

The idea that noncrop habitat enhances pest control and represents a win-win opportunity to conserve biodiversity and bolster yields has emerged as an agroecological paradigm. However, while noncrop habitat in landscapes surrounding farms sometimes benefits pest predators, natural enemy responses remain heterogeneous across studies and effects on pests are inconclusive. The observed heterogeneity in species responses to noncrop habitat may be biological in origin or could result from variation in how habitat and biocontrol are measured. Here, we use a pest-control database encompassing 132 studies and 6,759 sites worldwide to model natural enemy and pest abundances, predation rates, and crop damage as a function of landscape composition. Our results showed that although landscape composition explained significant variation within studies, pest and enemy abundances, predation rates, crop damage, and yields each exhibited different responses across studies, sometimes increasing and sometimes decreasing in landscapes with more noncrop habitat but overall showing no consistent trend. Thus, models that used landscape-composition variables to predict pest-control dynamics demonstrated little potential to explain variation across studies, though prediction did improve when comparing studies with similar crop and landscape features. Overall, our work shows that surrounding noncrop habitat does not consistently improve pest management, meaning habitat conservation may bolster production in some systems and depress yields in others. Future efforts to develop tools that inform farmers when habitat conservation truly represents a win-win would benefit from increased understanding of how landscape effects are modulated by local farm management and the biology of pests and their enemies.

Resource allocation trade-offs and the loss of chemical defences during apple domestication.

BACKGROUND AND AIMS: Most crops have been dramatically altered from their wild ancestors with the primary goal of increasing harvestable yield. A long-held hypothesis is that increased allocation to yield has reduced plant investment in defence and resulted in crops that are highly susceptible to pests. However, clear demonstrations of these trade-offs have been elusive due to the many selective pressures that occur concurrently during crop domestication. METHODS: To provide a robust test of whether increased allocation to yield can alter plant investment in defence, this study examined fruit chemical defence traits and herbivore resistance across 52 wild and 56 domesticated genotypes of apples that vary >26-fold in fruit size. Ninety-six phenolic metabolites were quantified in apple skin, pulp and seeds, and resistance to the codling moth was assessed with a series of bioassays. KEY RESULTS: The results show that wild apples have higher total phenolic concentrations and a higher diversity of metabolites than domesticated apples in skin, pulp and seeds. A negative phenotypic relationship between fruit size and phenolics indicates that this pattern is driven in part by allocation-based trade-offs between yield and defence. There were no clear differences in codling moth performance between wild and domesticated apples and no overall effects of total phenolic concentration on codling moth performance, but the results did show that codling moth resistance was increased in apples with higher phenolic diversity. The concentrations of a few individual compounds (primarily flavan-3-ols) also correlated with increased resistance, primarily driven by a reduction in pupal mass of female moths. CONCLUSIONS: The negative phenotypic relationship between fruit size and phenolic content, observed across a large number of wild and domesticated genotypes, supports the hypothesis of yield-defence trade-offs in crops. However, the limited effects of phenolics on codling moth highlight the complexity of consequences that domestication has for plant-herbivore interactions. Continued studies of crop domestication can further our understanding of the multiple trade-offs involved in plant defence, while simultaneously leading to novel discoveries that can improve the sustainability of crop production.

Landscape context shifts the balance of costs and benefits from wildflower borders on multiple ecosystem services.

In the face of global biodiversity declines driven by agricultural intensification, local diversification practices are broadly promoted to support farmland biodiversity and multiple ecosystem services. The creation of flower-rich habitats on farmland has been subsidized in both the USA and EU to support biodiversity and promote delivery of ecosystem services. Yet, theory suggests that the landscape context in which local diversification strategies are implemented will influence their success. However, few studies have empirically evaluated this theory or assessed the ability to support multiple ecosystem services simultaneously. Here, we evaluate the impact of creating flower-rich habitats in field margins on pollination, pest control, and crop yield over 3 years using a paired design across a landscape gradient. We find general positive effects of natural habitat cover on fruit weight and that flowering borders increase yields by promoting bee visitation to adjacent crops only in landscapes with intermediate natural habitat cover. Flowering borders had little impact on biological control regardless of landscape context. Thus, knowledge of landscape context can be used to target wildflower border placement in areas where they will have the greatest likelihood for success and least potential for increasing pest populations or yield loss in nearby crops.

Can overcompensation increase crop production?

The two most pressing challenges to agriculture worldwide are feeding a rapidly growing human population and developing more sustainable agricultural practices that do not threaten human and ecosystem health. We address these challenges through research in plant-herbivore interactions, specifically overcompensatory responses in potato to herbivore damage. While herbivory is usually detrimental to most crops, some potato cultivars can overcompensate and increase crop productivity up to two-fold in response to herbivore damage. However, biotic and abiotic factors are known to influence compensatory responses. Here we tested if compensatory plant responses to herbivory increase productivity of potatoes under field conditions along gradients of altitude and landscape simplification in 15 different farms. Our results suggest that compensatory plant responses could double the mean productivity of a potato farm in relation to the productivity of undamaged plants. The compensatory response is best predicted by pest pressure on a farm with potato plants having the maximum productivity when 10% of the tubers are damaged and decreasing in productivity as pest pressure increases. To a lesser extent an interaction between altitude and landscape simplification did affect the compensatory response, suggesting that abiotic factors play an important role in compensation. Our results suggest that overcompensation-based management practices could be used to maximize yields on working potato farms. Further research is required to determine action thresholds (i.e. the damage levels at which pest control needs to be enacted to maximize yields and minimize insecticide use) to develop more sustainable ways of increasing yields in the future.

Landscape simplification reduces classical biological control and crop yield.

Agricultural intensification resulting in the simplification of agricultural landscapes is known to negatively impact the delivery of key ecosystem services such as the biological control of crop pests. Both conservation and classical biological control may be influenced by the landscape context in which they are deployed; yet studies examining the role of landscape structure in the establishment and success of introduced natural enemies and their interactions with native communities are lacking. In this study, we investigated the relationship between landscape simplification, classical and conservation biological control services and importantly, the outcome of these interactions for crop yield. We showed that agricultural simplification at the landscape scale is associated with an overall reduction in parasitism rates of crop pests. Additionally, only introduced parasitoids were identified, and no native parasitoids were found in crop habitat, irrespective of agricultural landscape simplification. Pest densities in the crop were lower in landscapes with greater proportions of semi-natural habitats. Furthermore, farms with less semi-natural cover in the landscape and consequently, higher pest numbers, had lower yields than farms in less agriculturally dominated landscapes. Our study demonstrates the importance of landscape scale agricultural simplification in mediating the success of biological control programs and highlights the potential risks to native natural enemies in classical biological control programs against native insects. Our results represent an important contribution to an understanding of the landscape-mediated impacts on crop yield that will be essential to implementing effective policies that simultaneously conserve biodiversity and ecosystem services.

Contrasting effects of landscape composition on crop yield mediated by specialist herbivores.

Landscape composition not only affects a variety of arthropod-mediated ecosystem services, but also disservices, such as herbivory by insect pests that may have negative effects on crop yield. Yet, little is known about how different habitats influence the dynamics of multiple herbivore species, and ultimately their collective impact on crop production. Using cabbage as a model system, we examined how landscape composition influenced the incidence of three specialist cruciferous pests (aphids, flea beetles, and leaf-feeding Lepidoptera), lepidopteran parasitoids, and crop yield across a gradient of landscape composition in New York, USA. We expected that landscapes with a higher proportion of cropland and lower habitat diversity would lead to an increase in pest pressure of the specialist herbivores and a reduction in crop yield. However, results indicated that neither greater cropland area nor lower landscape diversity influenced pest pressure or yield. Rather, pest pressure and yield were best explained by the presence of non-crop habitats (i.e., meadows) in the landscape. Specifically, cabbage was infested with fewer Lepidoptera in landscapes with a higher proportion of meadows likely resulting from increased parasitism. Conversely, cabbage was infested with more flea beetles and aphids as the proportion of meadows in the landscape increased, suggesting that these pests benefit from non-crop habitats. Furthermore, path analysis confirmed that these landscape-mediated effects on pest populations can have either positive or negative cascading effects on crop yield. Our findings illustrate how different pest species within the same cropping system show contrasting responses to landscape composition with respect to both the direction and spatial scale of the relationship. Such tradeoffs resulting from the complex interaction between multiple-pests, natural enemies, and landscape composition must be considered, if we are to manage landscapes for pest suppression benefits.

Tecia solanivora infestation increases tuber starch accumulation in Pastusa Suprema potatoes.

In response to infestation with larvae of the Guatemalan tuber moth (Tecia solanivora), some Solanum tuberosum (potato) varieties exhibit an overcompensation response, whereby the total dry mass of uninfested tubers is increased. Here, we describe early responses, within the first few days, of T. solanivora feeding, in the Colombian potato variety Pastusa Suprema. Non-targeted metabolite profiling showed significant secondary metabolism changes in T. solanivora-infested tubers, but not in uninfested systemic tubers. In contrast, changes in primary metabolism were greater in uninfested systemic tubers than in the infested tubers, with a notable 80% decline in systemic tuber sucrose levels within 1 d of T. solanivora infestation. This suggested either decreased sucrose transport from the leaves or increased sink strength, i.e., more rapid sucrose to starch conversion in the tubers. Increased sucrose synthesis was indicated by higher rubisco activase and lower starch synthase gene expression in the leaves of infested plants. Elevated sink strength was demonstrated by 45% more total starch deposition in systemic tubers of T. solanivora-infested plants compared to uninfested control plants. Thus, rather than investing in increased defense of uninfested tubers, Pastusa Suprema promotes deposition of photoassimilates in the form of starch as a response to T. solanivora infestation.

A global synthesis of the effects of diversified farming systems on arthropod diversity within fields and across agricultural landscapes.

Agricultural intensification is a leading cause of global biodiversity loss, which can reduce the provisioning of ecosystem services in managed ecosystems. Organic farming and plant diversification are farm management schemes that may mitigate potential ecological harm by increasing species richness and boosting related ecosystem services to agroecosystems. What remains unclear is the extent to which farm management schemes affect biodiversity components other than species richness, and whether impacts differ across spatial scales and landscape contexts. Using a global metadataset, we quantified the effects of organic farming and plant diversification on abundance, local diversity (communities within fields), and regional diversity (communities across fields) of arthropod pollinators, predators, herbivores, and detritivores. Both organic farming and higher in-field plant diversity enhanced arthropod abundance, particularly for rare taxa. This resulted in increased richness but decreased evenness. While these responses were stronger at local relative to regional scales, richness and abundance increased at both scales, and richness on farms embedded in complex relative to simple landscapes. Overall, both organic farming and in-field plant diversification exerted the strongest effects on pollinators and predators, suggesting these management schemes can facilitate ecosystem service providers without augmenting herbivore (pest) populations. Our results suggest that organic farming and plant diversification promote diverse arthropod metacommunities that may provide temporal and spatial stability of ecosystem service provisioning. Conserving diverse plant and arthropod communities in farming systems therefore requires sustainable practices that operate both within fields and across landscapes.

The Effects of Plant Compensatory Regrowth and Induced Resistance on Herbivore Population Dynamics.

Outbreaks of herbivorous insects are detrimental to natural and agricultural systems, but the mechanisms driving outbreaks are not well understood. Plant responses to herbivory have the potential to produce outbreaks, but long-term effects of plant responses on herbivore dynamics are understudied. To quantify these effects, we analyze mathematical models of univoltine herbivores consuming annual plants with two responses: (1) compensatory regrowth, which affects herbivore survival in food-limited situations by increasing the amount of food available to the herbivore; and (2) induced resistance, which reduces herbivore survival proportional to the strength of the response. Compensatory regrowth includes tolerance, where plants replace some or all of the consumed biomass, and overcompensation, where plants produce more biomass than was consumed. We found that overcompensation can cause bounded fluctuations in the herbivore density (called outbreaks here) by itself, whereas neither tolerance nor induced resistance can cause an outbreak on its own. Food limitation and induced resistance can also drive outbreaks when they act simultaneously. Tolerance damps these outbreaks, but overcompensation, by contrast, qualitatively changes the conditions under which the outbreaks occur. Not properly accounting for these interactions may explain why it has been difficult to document plant-driven insect outbreaks and could undermine efforts to control herbivore populations in agricultural systems.

Potato tuber herbivory increases resistance to aboveground lepidopteran herbivores.

Plants mediate interactions between aboveground and belowground herbivores. Although effects of root herbivory on foliar herbivores have been documented in several plant species, interactions between tuber-feeding herbivores and foliar herbivores are rarely investigated. We report that localized tuber damage by Tecia solanivora (Guatemalan tuber moth) larvae reduced aboveground Spodoptera exigua (beet armyworm) and Spodoptera frugiperda (fall armyworm) performance on Solanum tuberosum (potato). Conversely, S. exigua leaf damage had no noticeable effect on belowground T. solanivora performance. Tuber infestation by T. solanivora induced systemic plant defenses and elevated resistance to aboveground herbivores. Lipoxygenase 3 (Lox3), which contributes to the synthesis of plant defense signaling molecules, had higher transcript abundance in T. solanivora-infested leaves and tubers than in equivalent control samples. Foliar expression of the hydroxycinnamoyl-CoA quinate hydroxycinnamoyl transferase (HQT) and 3-hydroxy-3-methylglutaryl CoA reductase I (HMGR1) genes, which are involved in chlorogenic acid and steroidal glycoalkaloid biosynthesis, respectively, also increased in response to tuber herbivory. Leaf metabolite profiling demonstrated the accumulation of unknown metabolites as well as the known potato defense compounds chlorogenic acid, α-solanine, and α-chaconine. When added to insect diet at concentrations similar to those found in potato leaves, chlorogenic acid, α-solanine, and α-chaconine all reduced S. exigua larval growth. Thus, despite the fact that tubers are a metabolic sink tissue, T. solanivora feeding elicits a systemic signal that induces aboveground resistance against S. exigua and S. frugiperda by increasing foliar abundance of defensive metabolites.

The raison d'être of chemical ecology.

Chemical ecology is a mechanistic approach to understanding the causes and consequences of species interactions, distribution, abundance, and diversity. The promise of chemical ecology stems from its potential to provide causal mechanisms that further our understanding of ecological interactions and allow us to more effectively manipulate managed systems. Founded on the notion that all organisms use endogenous hormones and chemical compounds that mediate interactions, chemical ecology has flourished over the past 50 years since its origin. In this essay we highlight the breadth of chemical ecology, from its historical focus on pheromonal communication, plant-insect interactions, and coevolution to frontier themes including community and ecosystem effects of chemically mediated species interactions. Emerging approaches including the -omics, phylogenetic ecology, the form and function of microbiomes, and network analysis, as well as emerging challenges (e.g., sustainable agriculture and public health) are guiding current growth of this field. Nonetheless, the directions and approaches we advocate for the future are grounded in classic ecological theories and hypotheses that continue to motivate our broader discipline.

Herbivore and pollinator body size effects on strawberry fruit quality.

Land use change affects both pollinator and herbivore populations with consequences for crop production. Recent evidence also shows that land use change affects insect traits, with intraspecific body size of pollinators changing across landscape gradients. However, the consequences on crop production of trait changes in different plant interactors have not been well-studied. We hypothesized that changes in body size of key species can be enough to affect crop productivity, and therefore looked at how the field-realistic variation in body size of both an important pollinator, Bombus impatiens (Cresson), and a key pest herbivore, Lygus lineolaris (Palisot), can affect fruit size and damage in strawberry. First, we determined if pests vary in body size along land use gradients as prior studies have documented for pollinators; and second, we tested under controlled conditions how the individual and combined changes in size of an important pollinator and a key herbivore pest affect strawberry fruit production. The key herbivore pest was smaller in landscapes with more natural and semi-natural habitat, confirming that herbivore functional traits can vary along a land use gradient. Additionally, herbivore size, and not pollinator size, marginally affected fruit production-with plants exposed to larger pests producing smaller fruits. Our findings suggest that land use changes at the landscape level affect crop production not just through changes in the species diversity of insect communities that interact with the plant, but also through changes in body size traits.

Agricultural landscape simplification affects wild plant reproduction indirectly through herbivore-mediated changes in floral display.

As natural landscapes are modified and converted into simplified agricultural landscapes, the community composition and interactions of organisms persisting in these modified landscapes are altered. While many studies examine the consequences of these changing interactions for crops, few have evaluated the effects on wild plants. Here, we examine how pollinator and herbivore interactions affect reproductive success for wild resident and phytometer plants at sites along a landscape gradient ranging from natural to highly simplified. We tested the direct and indirect effects of landscape composition on plant traits and reproduction mediated by insect interactions. For phytometer plants exposed to herbivores, we found that greater landscape complexity corresponded with elevated herbivore damage, which reduced total flower production but increased individual flower size. Though larger flowers increased pollination, the reduction in flowers ultimately reduced plant reproductive success. Herbivory was also higher in complex landscapes for resident plants, but overall damage was low and therefore did not have a cascading effect on floral display and reproduction. This work highlights that landscape composition directly affects patterns of herbivory with cascading effects on pollination and wild plant reproduction. Further, the absence of an effect on reproduction for resident plants suggests that they may be adapted to their local insect community.

Route of exposure to veterinary products in bees: Unraveling pasture's impact on avermectin exposure and tolerance in stingless bees.

Deforestation rapidly increases in tropical regions, primarily driven by converting natural habitats into pastures for extensive cattle ranching. This landscape transformation, coupled with pesticide use, are key drivers of bee population decline. Here, we investigate the impact of pasture-dominated landscapes on colony performance, pesticide exposure, and insecticide sensitivity of the stingless bee Tetragonisca angustula. We monitored 16 colonies located in landscapes with varying proportions of pasture. We collected bee bread for pesticide and palynological analysis. We found a positive correlation between pollen diversity and colony growth, with no effect of the proportion of pasture in the landscape. In contrast, we detected prevalent and hazardous concentrations of the insecticide abamectin (9.6-1,856 µg/kg) in bee bread, which significantly increased with a higher proportion of pasture. Despite the abamectin exposure, the bee colonies displayed no adverse effects on their growth, indicating a potential tolerance response. Further investigations revealed that bees from sites with higher proportions of pasture showed significantly reduced mortality when exposed to a lethal concentration of abamectin (0.021 µg/µL) after 48 h. Since abamectin is scarcely used in the study area, we designed an experiment to track ivermectin, a closely related antiparasitic drug used in cattle. Our findings uncovered a new exposure route of bees to pesticides, wherein ivermectin excreted by cattle is absorbed and biotransformed into abamectin within flowering plants in the pastures. These results highlight that unexplained exposure routes of bees to pesticides remain to be described while also revealing that bees adapt to changing landscapes.

Phenotypic clines in herbivore resistance and reproductive traits in wild plants along an agricultural gradient.

The conversion of natural landscapes to agriculture is a leading cause of biodiversity loss worldwide. While many studies examine how landscape modification affects species diversity, a trait-based approach can provide new insights into species responses to environmental change. Wild plants persisting in heavily modified landscapes provide a unique opportunity to examine species' responses to land use change. Trait expression within a community plays an important role in structuring species interactions, highlighting the potential implications of landscape mediated trait changes on ecosystem functioning. Here we test the effect of increasing agricultural landscape modification on defensive and reproductive traits in three commonly occurring Brassicaceae species to evaluate plant responses to landscape change. We collected seeds from populations at spatially separated sites with variation in surrounding agricultural land cover and grew them in a greenhouse common garden, measuring defensive traits through an herbivore no-choice bioassay as well as reproductive traits such as flower size and seed set. In two of the three species, plants originating from agriculturally dominant landscapes expressed a consistent reduction in flower size and herbivore leaf consumption. One species also showed reduced fitness associated with increasingly agricultural landscapes. These findings demonstrate that wild plants are responding to landscape modification, suggesting that the conversion of natural landscapes to agriculture has consequences for wild plant evolution.

The pest control and pollinator protection dilemma: The case of thiamethoxam prophylactic applications in squash crops.

A major challenge in sustainable agriculture is finding solutions to manage crop-damaging pests such as herbivores while protecting beneficial organisms such as pollinators. Squash is a highly pollinator-dependent crop that is also attractive to herbivores like the striped cucumber beetle. While synthetic insecticides can provide control of insect pests, they can also affect non-target organisms such as pollinators. Thus, growers need to balance pest management with pollinator protection to ensure optimal yield. Thiamethoxam is a commonly used systemic insecticide that translocates throughout plants, leaving residues in nectar and pollen. The aim of this study was to evaluate whether there are uses of this insecticide that provides efficient pest control while minimizing pesticide pollinator exposure. Specifically, we tested how different prophylactic application methods (seed treatments, in-furrow applications, and early foliar sprays) of commercially available thiamethoxam products impact pest control, bee visitation, yield, and pesticide residues in flowers of squash crops. We found that among the different methods of thiamethoxam application, in-furrow application best prevented defoliation and resulted in the highest fruit weight and number. However, it also produced the most frequent and highest concentrations of thiamethoxam in nectar and pollen, reaching lethal levels for squash bees. Our study provides evidence that under current application methods, thiamethoxam does not provide a sustainable solution for squash growers and further research is required on more efficient pesticide delivery methods, as well as non-pesticide pest control measurements.