Emily A. Martin

Natural enemy interactions constrain pest control in complex agricultural landscapes

Biological control of pests by natural enemies is a major ecosystem service delivered to agriculture worldwide. Quantifying and predicting its effectiveness at large spatial scales is critical for increased sustainability of agricultural production. Landscape complexity is known to benefit natural enemies, but its effects on interactions between natural enemies and the consequences for crop damage and yield are unclear. Here, we show that pest control at the landscape scale is driven by differences in natural enemy interactions across landscapes, rather than by the effectiveness of individual natural enemy guilds. In a field exclusion experiment, pest control by flying insect enemies increased with landscape complexity. However, so did antagonistic interactions between flying insects and birds, which were neutral in simple landscapes and increasingly negative in complex landscapes. Negative natural enemy interactions thus constrained pest control in complex landscapes. These results show that, by altering natural enemy interactions, landscape complexity can provide ecosystem services as well as disservices. Careful handling of the tradeoffs among multiple ecosystem services, biodiversity, and societal concerns is thus crucial and depends on our ability to predict the functional consequences of landscape-scale changes in trophic interactions.

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.

Scale‐dependent effects of landscape composition and configuration on natural enemy diversity, crop herbivory, and yields

(1) Land-use intensification in agricultural landscapes has led to changes in the way habitats and resources are distributed in space. Pests and their natural enemies are influenced by these changes, and by the farming intensity of crop fields. However, it is unknown whether the composition of landscapes (amount and diversity of land cover types) or their configuration (spatial arrangement of cover types) are more important for natural enemy diversity, and how they impact crop damage and yields. In addition, effects of interactions between local farming practices (organic vs. conventional) and landscape variables are unclear. (2) Here, we make use of a data set where landscape composition and configuration were uncorrelated across multiple spatial scales. Natural enemies, crop damage, and yields were sampled in 35 organic and conventional crop fields. Out of seven broad natural enemy taxa, five were positively affected by a complex landscape configuration. In contrast, only carabids were positively affected by the amount of seminatural habitat around fields. Increasing diversity of land cover types had positive effects on some, but negative effects on other taxa. Effect sizes varied among taxa but increased with increasing spatial scale, defined by circular areas of increasing radius around fields. (3) The diversity of aerial, but not of ground-dwelling enemies was higher in fields under organic than conventional management. Interactions of local and landscape variables were important for birds, but not other enemies. Bird richness was higher in organic fields in simple landscapes, but not in landscapes with complex configuration or high land cover diversity. (4) Crop damage decreased with landscape diversity, but increased in conventional fields with complex configuration. Yields increased with both parameters in conventional fields only, and were higher on average in organic compared to conventional fields. Enemy diversity was positively related to crop damage, indicating positive density-dependence of enemies on pests. However, the diversity of aerial enemies was also positively related to yields. (5) Our results suggest that the effectiveness of agrienvironmental schemes for managing natural enemy diversity, crop damage and yields could be enhanced by optimizing the effects of distinct landscape parameters, particularly landscape configuration and diversity, across scales.

Pest control of aphids depends on landscape complexity and natural enemy interactions

Aphids are a major concern in agricultural crops worldwide, and control by natural enemies is an essential component of the ecological intensification of agriculture. Although the complexity of agricultural landscapes is known to influence natural enemies of pests, few studies have measured the degree of pest control by different enemy guilds across gradients in landscape complexity. Here, we use multiple natural-enemy exclosures replicated in 18 fields across a gradient in landscape complexity to investigate (1) the strength of natural pest control across landscapes, measured as the difference between pest pressure in the presence and in the absence of natural enemies; (2) the differential contributions of natural enemy guilds to pest control, and the nature of their interactions across landscapes. We show that natural pest control of aphids increased up to six-fold from simple to complex landscapes. In the absence of pest control, aphid population growth was higher in complex than simple landscapes, but was reduced by natural enemies to similar growth rates across all landscapes. The effects of enemy guilds were landscape-dependent. Particularly in complex landscapes, total pest control was supplied by the combined contribution of flying insects and ground-dwellers. Birds had little overall impact on aphid control. Despite evidence for intraguild predation of flying insects by ground-dwellers and birds, the overall effect of enemy guilds on aphid control was complementary. Understanding pest control services at large spatial scales is critical to increase the success of ecological intensification schemes. Our results suggest that, where aphids are the main pest of concern, interactions between natural enemies are largely complementary and lead to a strongly positive effect of landscape complexity on pest control. Increasing the availability of seminatural habitats in agricultural landscapes may thus benefit not only natural enemies, but also the effectiveness of aphid natural pest control.

Combined effects of agrochemicals and ecosystem services on crop yield across Europe

Simultaneously enhancing ecosystem services provided by biodiversity below and above ground is recommended to reduce dependence on chemical pesticides and mineral fertilisers in agriculture. However, consequences for crop yield have been poorly evaluated. Above ground, increased landscape complexity is assumed to enhance biological pest control, whereas below ground, soil organic carbon is a proxy for several yield-supporting services. In a field experiment replicated in 114 fields across Europe, we found that fertilisation had the strongest positive effect on yield, but hindered simultaneous harnessing of below- and above-ground ecosystem services. We furthermore show that enhancing natural enemies and pest control through increasing landscape complexity can prove disappointing in fields with low soil services or in intensively cropped regions. Thus, understanding ecological interdependences between land use, ecosystem services and yield is necessary to promote more environmentally friendly farming by identifying situations where ecosystem services are maximised and agrochemical inputs can be reduced.

Enhancing Soil Organic Matter as a Route to the Ecological Intensification of European Arable Systems

Abstract Soil organic matter (SOM) is declining in most agricultural ecosystems, impacting multiple ecosystem services including erosion and flood prevention, climate and greenhouse gas regulation as well as other services that underpin crop production, such as nutrient cycling and pest control. Ecological intensification aims to enhance crop productivity by including regulating and supporting ecosystem service management into agricultural practices. We investigate the potential for increased SOM to support the ecological intensification of arable systems by reducing the need for nitrogen fertiliser application and pest control. Using a large-scale European field trial implemented across 84 fields in 5 countries, we tested whether increased SOM (using soil organic carbon as a proxy) helps recover yield in the absence of conventional nitrogen fertiliser and whether this also supports crops less favourable to key aphid pests. Greater SOM increased yield by 10%, but did not offset nitrogen fertiliser application entirely, which improved yield by 30%. Crop pest responses depended on species: Metopolophium dirhodum were more abundant in fertilised plots with high crop biomass, and although population growth rates of Sitobion avenae were enhanced by nitrogen fertiliser application in a cage trial, field populations were not affected. We conclude that under increased SOM and reduced fertiliser application, pest pressure can be reduced, while partially compensating for yield deficits linked to fertiliser reduction. If the benefits of reduced fertiliser application and increased SOM are considered in a wider environmental context, then a yield cost may become acceptable. Maintaining or increasing SOM is critical for achieving ecological intensification of European cereal production.

Investigating the (Mis)Match between Natural Pest Control Knowledge and the Intensity of Pesticide Use

Transforming modern agriculture towards both higher yields and greater sustainability is critical for preserving biodiversity in an increasingly populous and variable world. However, the intensity of agricultural practices varies strongly between crop systems. Given limited research capacity, it is crucial to focus efforts to increase sustainability in the crop systems that need it most. In this study, we investigate the match (or mismatch) between the intensity of pesticide use and the availability of knowledge on the ecosystem service of natural pest control across various crop systems. Using a systematic literature search on pest control and publicly available pesticide data, we find that pest control literature is not more abundant in crops where insecticide input per hectare is highest. Instead, pest control literature is most abundant, with the highest number of studies published, in crops with comparatively low insecticide input per hectare but with high world harvested area. These results suggest that a major increase of interest in agroecological research towards crops with high insecticide input, particularly cotton and horticultural crops such as citrus and high value-added vegetables, would help meet knowledge needs for a timely ecointensification of agriculture.

High highs and low lows: Elucidating striking seasonal variability in pesticide use and its environmental implications

Despite substantial public and scientific concern regarding unintended environmental and health consequences of agricultural pesticide use, identifying when and where high levels of use occur is stymied by a dearth of data at biologically relevant spatial or temporal scales. Here we investigate intra-annual patterns in pesticide use by crop and by pesticide type using unique pesticide use data from agriculturally diverse croplands of California, USA. We find that timing and type of pesticide use is strongly crop-dependent, and that for many high pesticide use crops, monthly application rates are highly consistent from year-to-year. Further, while pesticide use hotspots are concentrated in early summer, regions with very high use occur throughout the year with spatial distributions varying therein. The enormity of intra-annual variation in pesticide use, as well as the consistency in those patterns through time, suggests opportunities for crop-specific pest management and region-specific mitigation approaches to limit environmental and human health hazards from agricultural pesticide use.

Landscape heterogeneity rather than crop diversity mediates bird diversity in agricultural landscapes

Crop diversification has been proposed as farm management tool that could mitigate the externalities of conventional farming while reducing productivity-biodiversity trade-offs. Yet evidence for the acclaimed biodiversity benefits of landscape-level crop diversity is ambiguous. Effects may strongly depend on spatial scale and the level of landscape heterogeneity (e.g. overall habitat diversity). At the same time, contrasting within-taxon responses obscure benefits to specific functional groups (i.e. species with shared characteristics or requirements) if studied at the community level. The objectives of this study were to 1) disentangle the relative effects of crop diversity and landscape heterogeneity on avian species richness across five spatial scales ranging from 250 to 3000 m radii around focal winter wheat fields; and 2) assess whether functional groups (feeding guild, conservation status, habitat preference, nesting behaviour) determine the strength and direction of responses to crop diversity and landscape heterogeneity. In central Germany, 14 landscapes were selected along independent gradients of crop diversity (annual arable crops) and landscape heterogeneity. Bird species richness in each landscape was estimated using four point counts throughout the breeding season. We found no effects of landscape-level crop diversity on bird richness and functional groups. Instead, landscape heterogeneity was strongly associated with increased total bird richness across all spatial scales. In particular, insect-feeding and non-farmland birds were favoured in heterogeneous landscapes, as were species not classified as endangered or vulnerable on the regional Red List. Crop-nesting farmland birds, however, were less species-rich in these landscapes. Accordingly, crop diversification may be less suitable for conserving avian diversity and associated ecosystem services (e.g. biological pest control), although confounding interactions with management intensity need yet to be confirmed. In contrast, enhancement of landscape heterogeneity by increasing perennial habitat diversity, reducing field sizes and the amount of cropland has the potential to benefit overall bird richness. Specialist farmland birds, however, may require more targeted management approaches.