Distance functions of carabids in crop fields depend on functional traits, crop type and adjacent habitat: a synthesis.

Natural pest and weed regulation are essential for agricultural production, but the spatial distribution of natural enemies within crop fields and its drivers are mostly unknown. Using 28 datasets comprising 1204 study sites across eight Western and Central European countries, we performed a quantitative synthesis of carabid richness, activity densities and functional traits in relation to field edges (i.e. distance functions). We show that distance functions of carabids strongly depend on carabid functional traits, crop type and, to a lesser extent, adjacent non-crop habitats. Richness of both carnivores and granivores, and activity densities of small and granivorous species decreased towards field interiors, whereas the densities of large species increased. We found strong distance decays in maize and vegetables whereas richness and densities remained more stable in cereals, oilseed crops and legumes. We conclude that carabid assemblages in agricultural landscapes are driven by the complex interplay of crop types, adjacent non-crop habitats and further landscape parameters with great potential for targeted agroecological management. In particular, our synthesis indicates that a higher edge-interior ratio can counter the distance decay of carabid richness per field and thus likely benefits natural pest and weed regulation, hence contributing to agricultural sustainability.

Increasing landscape heterogeneity as a win-win solution to manage trade-offs in biological control of crop and woodland pests.

Agriculture and forestry cover more than 75% of Europe, and invertebrate pests are a costly challenge for these two economic sectors. Landscape management is increasingly promoted as a solution to enhance biological pest control, but little is known on its effects on adjacent crop fields and woodlands. This study aims to explore the effect of the proportion of woodlands and permanent grasslands as well as crop diversity on biological pest control simultaneously in cereals fields and woodland patches, in south-western France. We used different types of sentinel prey as well as bird and carabid community metrics to assess biological pest control potential in these two ecosystems. We first show that land cover variables influence biological pest control both in cereal fields and woodland patches, but have antagonistic effects in the two ecosystems. Although results vary according to the biological control indicator considered, we show that increasing landscape heterogeneity represents a valuable solution to manage trade-offs and promote higher average predation rates across forests and cereal fields. Our study therefore calls for more integrative studies to identify landscape management strategies that enable nature-based solutions across ecosystems.

Inconsistent responses of conservation biocontrol to landscape structure: new insights from a network-based review.

Conservation biological control (CBC) has been an active research topic for the last two decades and is now one of the key ways being explored to develop agroecological production systems. Using broad concepts and indicators, recent reviews and meta-analyses have highlighted major inconsistencies in the responses of CBC to landscape structure, revealing their context-dependent nature. To decipher these relations, we reviewed the scientific literature (50 articles) using (1) an original ontology allowing us to navigate across the different terms and concepts used in this literature and (2) a network-based methodology to describe the scattering, completeness, and generalizability of scientific knowledge on CBC. An interactive version of this network is available online. Our results highlight the strong information scattering caused by the variety of indicators used to describe both landscape structure and CBC. We observe trade-offs between the use of coarse concepts classically used in meta-analysis (e.g., landscape complexity) and the non-convergence of results (ambiguity). The network analysis points out consistently less information ambiguity when considering sub-networks focused on trophic chains than in the full information network, without losing connectance. We suggest that effects of landscape structure may be different between trophic chains because of specific selection pressures associated with cropping systems. Our novel review procedure offers a relatively simple but powerful complementary approach to classical meta-analysis to explore ecological patterns. It highlights that crop trophic chain probably represents the adequate ecological unit to investigate the landscape-CBC relationship. Designing pest suppressive landscapes while favoring farmland biodiversity will imply considering multiple crop trophic chains responding differently to landscape structure. Therefore, we recommend assessing the level of CBC at both crop field and landscape scales to inform decisions on the best individual or collective strategy to adopt.

Wooded Semi-Natural Habitats Complement Permanent Grasslands in Supporting Wild Bee Diversity in Agricultural Landscapes.

Loss of semi-natural habitats (SNH) in agricultural landscapes affects wild bees, often negatively. However, how bee communities respond varies and is still unclear. To date, few studies have used precise descriptors to understand these effects. Our aim was to understand the respective and complementary influences of different wooded and herbaceous habitats on wild bee communities. We selected thirty 500-m radius landscapes on a gradient of a percentage of wooded SNH in south-western France. At each landscape, we sampled wild bees in spring 2016 and plants in spring 2015 and 2016 at the forest edge, in a hedgerow, and in a permanent grassland. Pollen carried by the most abundant bee species was collected and identified. Using beta diversity indices, we showed that wild bee community composition differs between the three SNH types, and especially between herbaceous and wooded SNH. Based on Jacobs' selection index, we showed that pollen of some plant species recorded in wooded SNH are preferentially selected by wild bees. Studying the impact of the loss of each SNH type on the global bee-pollen interaction network, we found that wooded SNH contributed to its resilience, enabling specific plant-bee interactions. Overall, our results underline the non-negligible contribution of wooded SNH to the diversity of wild bees in agricultural landscapes, and thus the importance of maintaining different types of SNH.

Tree diversity drives associational resistance to herbivory at both forest edge and interior.

Tree diversity is increasingly acknowledged as an important driver of insect herbivory. However, there is still a debate about the direction of associational effects that can range from associational resistance (i.e., less damage in mixed stands than in monocultures) to the opposite, associational susceptibility. Discrepancies among published studies may be due to the overlooked effect of spatially dependent processes such as tree location within forests. We addressed this issue by measuring crown defoliation and leaf damage made by different guilds of insect herbivores on oaks growing among conspecific versus heterospecific neighbors at forest edges versus interior, in two closed sites in SW France forests. Overall, oaks were significantly less defoliated among heterospecific neighbors (i.e., associational resistance), at both forest edge and interior. At the leaf level, guild diversity and leaf miner herbivory significantly increased with tree diversity regardless of oak location within stands. Other guilds showed no clear response to tree diversity or oak location. We showed that herbivore response to tree diversity varied among insect feeding guilds but not between forest edges and interior, with inconsistent patterns between sites. Importantly, we show that oaks were more defoliated in pure oak plots than in mixed plots at both edge and forest interior and that, on average, defoliation decreased with increasing tree diversity from one to seven species. We conclude that edge conditions could be interacting with tree diversity to regulate insect defoliation, but future investigations are needed to integrate them into the management of temperate forests, notably by better understanding the role of the landscape context.

Increasing crop heterogeneity enhances multitrophic diversity across agricultural regions.

Agricultural landscape homogenization has detrimental effects on biodiversity and key ecosystem services. Increasing agricultural landscape heterogeneity by increasing seminatural cover can help to mitigate biodiversity loss. However, the amount of seminatural cover is generally low and difficult to increase in many intensively managed agricultural landscapes. We hypothesized that increasing the heterogeneity of the crop mosaic itself (hereafter "crop heterogeneity") can also have positive effects on biodiversity. In 8 contrasting regions of Europe and North America, we selected 435 landscapes along independent gradients of crop diversity and mean field size. Within each landscape, we selected 3 sampling sites in 1, 2, or 3 crop types. We sampled 7 taxa (plants, bees, butterflies, hoverflies, carabids, spiders, and birds) and calculated a synthetic index of multitrophic diversity at the landscape level. Increasing crop heterogeneity was more beneficial for multitrophic diversity than increasing seminatural cover. For instance, the effect of decreasing mean field size from 5 to 2.8 ha was as strong as the effect of increasing seminatural cover from 0.5 to 11%. Decreasing mean field size benefited multitrophic diversity even in the absence of seminatural vegetation between fields. Increasing the number of crop types sampled had a positive effect on landscape-level multitrophic diversity. However, the effect of increasing crop diversity in the landscape surrounding fields sampled depended on the amount of seminatural cover. Our study provides large-scale, multitrophic, cross-regional evidence that increasing crop heterogeneity can be an effective way to increase biodiversity in agricultural landscapes without taking land out of agricultural production.

Biotic predictors complement models of bat and bird responses to climate and tree diversity in European forests.

Bats and birds are key providers of ecosystem services in forests. How climate and habitat jointly shape their communities is well studied, but whether biotic predictors from other trophic levels may improve bird and bat diversity models is less known, especially across large bioclimatic gradients. Here, we achieved multi-taxa surveys in 209 mature forests replicated in six European countries from Spain to Finland, to investigate the importance of biotic predictors (i.e. the abundance or activity of defoliating insects, spiders, earthworms and wild ungulates) for bat and bird taxonomic and functional diversity. We found that nine out of 12 bird and bat diversity metrics were best explained when biotic factors were added to models including climate and habitat variables, with a mean gain in explained variance of 38% for birds and 15% for bats. Tree functional diversity was the most important habitat predictor for birds, while bats responded more to understorey structure. The best biotic predictors for birds were spider abundance and defoliating insect activity, while only bat functional evenness responded positively to insect herbivory. Accounting for potential biotic interactions between bats, birds and other taxa of lower trophic levels will help to understand how environmental changes along large biogeographical gradients affect higher-level predator diversity in forest ecosystems.

Tree diversity reduces pest damage in mature forests across Europe.

Forest pest damage is expected to increase with global change. Tree diversity could mitigate this impact, but unambiguous demonstration of the diversity-resistance relationship is lacking in semi-natural mature forests. We used a network of 208 forest plots sampled along two orthogonal gradients of increasing tree species richness and latitudes to assess total tree defoliation in Europe. We found a positive relationship between tree species richness and resistance to insect herbivores: overall damage to broadleaved species significantly decreased with the number of tree species in mature forests. This pattern of associational resistance was frequently observed across tree species and countries, irrespective of their climate. These findings confirm the greater potential of mixed forests to face future biotic disturbances in a changing world.

Tree Diversity Limits the Impact of an Invasive Forest Pest.

The impact of invasive herbivore species may be lower in more diverse plant communities due to mechanisms of associational resistance. According to the "resource concentration hypothesis" the amount and accessibility of host plants is reduced in diverse plant communities, thus limiting the exploitation of resources by consumers. In addition, the "natural enemy hypothesis" suggests that richer plant assemblages provide natural enemies with more complementary resources and habitats, thus promoting top down regulation of herbivores. We tested these two hypotheses by comparing crown damage by the invasive Asian chestnut gall wasp (Dryocosmus kuriphilus) on chestnut trees (Castanea sativa) in pure and mixed stands in Italy. We estimated the defoliation on 70 chestnut trees in 15 mature stands sampled in the same region along a gradient of tree species richness ranging from one species (chestnut monocultures) to four species (mixtures of chestnut and three broadleaved species). Chestnut defoliation was significantly lower in stands with higher tree diversity. Damage on individual chestnut trees decreased with increasing height of neighboring, heterospecific trees. These results suggest that conservation biological control method based on tree species mixtures might help to reduce the impact of the Asian chestnut gall.

Migration and dispersal may drive to high genetic variation and significant genetic mixing: the case of two agriculturally important, continental hoverflies (Episyrphus balteatus and Sphaerophoria scripta).

Population structure of pests and beneficial species is an important issue when designing management strategies to optimize ecosystem services. In this study, we investigated for the first time the population structure at a continental scale of two migratory species of hoverflies providing both pest regulation and pollination services [Episyrphus balteatus and Sphaerophoria scripta (Diptera: Syrphidae)]. To achieve this objective, we used two sets of 12 species-specific microsatellite markers on a large-scale sampling from all over Europe. Our findings showed a high level of genetic mixing resulting in a lack of genetic differentiation at a continental scale and a great genetic diversity in the two species. All the pairwise FST values between European localities were less 0.05 in the two species. These low values reflect a large-scale genetic mixing probably caused by the existence of frequent migratory movements in the two species. Mantel tests revealed isolation-by-distance pattern on the East-West axis, but not on the North-South axis. This isolation-by-distance pattern confirms the existence of North-South migratory movements in both directions and suggests an important step by step dispersal. Population features shown by this study are common in invasive species and pests, but are not often observed in beneficial species. They reflect great colonization abilities and a high adaptive potential when dealing with a changing environment. Our results highlight the two studied species as particularly interesting beneficial insects for pollination and pest predation in the current context of global change.

Lack of genetic differentiation between contrasted overwintering strategies of a major pest predator Episyrphus balteatus (Diptera: Syrphidae): implications for biocontrol.

Winter ecology of natural enemies has a great influence on the level and efficiency of biological control at spring. The hoverfly Episyrphus balteatus (DeGeer) (Diptera: Syrphidae) is one of the most important natural predators of crop aphids in Europe. Three different overwintering strategies coexist in this species which makes it a good model in order to study ecologically-based speciation processes. The purpose of this study was to determine whether E. balteatus populations with alternative overwintering strategies are genetically differentiated. To that aim, we developed 12 specific microsatellite markers and evaluated the level of neutral genetic differentiation between E. balteatus field populations that overwinter in the three different ways described in this species (i.e. migration, local overwintering at a pre-imaginal stage, and local overwintering at adult stage). Results showed a lack of neutral genetic differentiation between individuals with different overwintering strategies although there are strong ecological differences between them. All pair-wise FST values are below 0.025 and non-significant, and Bayesian clustering showed K=1 was the most likely number of genetic clusters throughout our sample. The three overwintering strategies form one unique panmictic population. This suggests that all the individuals may have genetic material for the expression of different overwintering phenotypes, and that their commitment in one particular overwintering strategy may depend on environmental and individual factors. Consequently, the prevalence of the different overwintering strategies would be potentially modified by landscape engineering and habitat management which could have major implications for biological control.

Phytophagy on phylogenetically isolated trees: why hosts should escape their relatives.

Hosts belonging to the same species suffer dramatically different impacts from their natural enemies. This has been explained by host neighbourhood, that is, by surrounding host-species diversity or spatial separation between hosts. However, even spatially neighbouring hosts may be separated by many million years of evolutionary history, potentially reducing the establishment of natural enemies and their impact. We tested whether phylogenetic isolation of oak hosts from neighbouring trees within a forest canopy reduces phytophagy. We found that an increase in phylogenetic isolation by 100 million years corresponded to a 10-fold decline in phytophagy. This was not due to poorer living conditions for phytophages on phylogenetically isolated oaks. Neither species diversity of neighbouring trees nor spatial distance to the closest oak affected phytophagy. We suggest that reduced pressure by natural enemies is a major advantage for individuals within a host species that leave their ancestral niche and grow among distantly related species.

Phylogeography and historical demography of the Lusitanian snail Elona quimperiana reveal survival in unexpected separate glacial refugia.

BACKGROUND: Present day distributions of Palearctic taxa in northern latitudes mainly result from populations having survived in local patches during the Late Pleistocene and/or from recolonizing populations from southern temperate refugia. If well-studied Mediterranean and eastern European refugia are widely accepted, some recent biogeographical assumptions still remain unclear, such as the occurrence of multiple glacial refugia in Iberia and cryptic refugia in northern Europe during the last glaciations. The Lusitanian snail Elona quimperiana has a remarkably disjunct distribution, limited to northwestern France (Brittany), northwestern Spain and the Basque Country. By describing the phylogeographical structure of this species across its entire range, the present study attempts to identify refugia and subsequent recolonization routes. RESULTS: Results based on 16S and COI gene sequences showed that the low genetic diversity observed in the Brittany populations should be associated with a recent demographic expansion. By contrast, populations from Spain exhibit several differentiated lineages and are characterized by demographic equilibrium, while the Basque populations are the only ones harboring typical distinct haplotypes. The center of the star-like networks of both gene sequences is occupied by a common ancestral-like haplotype found in Brittany and Spain, which might have originated from the middle of Northern Spain (i.e. Asturias, eastern Lugo and western Cantabria). Estimates of the divergence time between the Spain-Brittany and Basque lineages strongly suggest that E. quimperiana survived the Pleistocene glaciations in distinct refugia on the Iberian Peninsula, one of which is situated in Picos de Europa, and the other in the Basque Country. The occurrence of a northern refugium in France cannot be rejected as of yet. CONCLUSION: Present results confirm the Iberian origin of the land snail E. quimperiana and strongly support the emerging phylogeographic hypothesis of multiple refugia in Iberia during the last glaciations. The scenario of a spatial expansion of E. quimperiana from an Iberian refuge located in Asturias to northern areas provides the most probable explanation for the present distribution of this land snail. By harboring distinct haplotypes, the Basque Country populations appear to be of great importance in terms of potential adaptation, long term persistence and hence, the conservation of E. quimperiana.

Tracing individual movements of aphids reveals preferential routes of population transfers in agroecosystems.

Agricultural pests are not restricted to crops, but often simultaneously or successively use different cultivated and uncultivated hosts. Nevertheless, the source-sink role of cultivated and uncultivated habitats in the life cycle of crop pests remains poorly understood. This is largely due to the difficulty of tracking displacements of small organisms in agricultural landscapes. We used stable-isotope ratios in order to infer the natal host plant of individuals of the English grain aphid Sitobion avenae colonizing wheat fields in autumn. We showed that among the numerous plant sources of S. avenae, maize, which has been intensively grown in western France since the 1960s, provided most aphids that attack wheat fields early in autumn. This study illustrates how insect pests respond to land-use changes within a relatively short period of time, rapidly acquiring a new host that in turn affected their population biology considerably by playing a pivotal role on their annual life cycle.

Limited genetic exchanges between populations of an insect pest living on uncultivated and related cultivated host plants.

Habitats in agroecosystems are ephemeral, and are characterized by frequent disturbances forcing pest species to successively colonize various hosts belonging either to the cultivated or to the uncultivated part of the agricultural landscape. The role of wild habitats as reservoirs or refuges for the aphid Sitobion avenae that colonize cultivated fields was assessed by investigating the genetic structure of populations collected on both cereal crops (wheat, barley and oat) and uncultivated hosts (Yorkshire fog, cocksfoot, bulbous oatgrass and tall oatgrass) in western France. Classical genetic analyses and Bayesian clustering algorithms indicate that genetic differentiation is high between populations collected on uncultivated hosts and on crops, revealing a relatively limited gene flow between the uncultivated margins and the cultivated part of the agroecosystem. A closer genetic relatedness was observed between populations living on plants belonging to the same tribe (Triticeae, Poeae and Aveneae tribes) where aphid genotypes appeared not to be specialized on a single host, but rather using a group of related plant species. Causes of this ecological differentiation and its implications for integrated pest management of S. avenae as cereals pest are discussed.

Improvement of Barley yellow dwarf virus-PAV detection in single aphids using a fluorescent real time RT-PCR.

One of the major factors determining the incidence of Barley yellow dwarf virus (BYDV) on autumn-sown cereals is the viruliferous state of immigrant winged aphids. This variable is assessed routinely using the enzyme-linked immunosorbant assay (ELISA). However, the threshold for virus detection by ELISA can lead to false negative results for aphids carrying less than 10(6) particles. Although molecular detection techniques enabling the detection of lower virus quantities in samples are available, the relatively laborious sample preparation and data analysis have restricted their use in routine applications. A gel-free real-time one-step reverse transcription polymerase chain reaction (RT-PCR) protocol is described for specific detection and quantitation of BYDV-PAV, the most widespread BYDV species in Western Europe. This new assay, based on TaqMan technology, detects and quantifies from 10(2) to 10(8) BYDV-PAV RNA copies. This test is 10 and 10(3) times more sensitive than the standard RT-PCR and ELISA assays published previously for BYDV-PAV detection and significantly improves virus detection in single aphids. Extraction of nucleic acids from aphids using either phenol/chloroform or chelatin resin-based protocols allow the use of pooled samples or of a small part (up to 1/1600th) of a single aphid extract for efficient BYDV-PAV detection.