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.

Predicting the seasonal flight activity of Myzus persicae, the main aphid vector of Virus Yellows in sugar beet.

BACKGROUND: Virus Yellows (VY), a disease caused by several aphid-borne viruses, is a major threat to the global sugar beet production. Following the ban of neonicotinoid-based seed treatments against aphids in Europe, increased efforts are needed to monitor and forecast aphid population spread during the sugar beet growing season. In particular, predicting aphid flight seasonal activity could allow anticipation of the timing and intensity of crop colonisation and contribute to the proper implementation of management methods. Forecasts should be made early enough to assess risk, but can be updated as the season progresses to refine management. Based on a long-term suction-trap dataset gathered between 1978 and 2014, we built and evaluated a set of models to predict the flight activity features of the main VY vector, Myzus persicae, at any location in the French sugar beet production area (c. 4 × 105 ha). Flight onset dates, length of flight period and cumulative abundance of flying aphids were predicted using climatic and land-use predictors as well as geographical position. RESULTS: Our predictions outperformed current models published in the literature. The importance of the predictor variables varied according to the predicted flight feature but winter and early spring temperature always played a major role. Forecasts based on temperature were made more accurate by adding predictors related to aphid winter reservoirs. In addition, updating the model parameters to take advantage of new weather data acquired during the season improved the flight forecast. CONCLUSION: Our models can be used as a tool for the mitigation in sugar beet crops. © 2023 Society of Chemical Industry.

Assessing spatial deposition of aquatic subsidies by insects emerging from agricultural streams.

The role of winged aquatic insects that emerge from streams and subsidize terrestrial ecosystems has been demonstrated for natural forest landscapes, but almost no information is available for intensive agricultural landscapes. This study is the first to estimate aquatic subsidies provided by flying insects that emerge from streams and land on cropland. We investigated three major groups of aquatic insects - Trichoptera, Ephemeroptera and Chironomidae (Diptera) - that emerged from 12 third-order temperate, agricultural streams. We simultaneously monitored their emergence using floating traps and their terrestrial dispersal using passive interception traps. We estimated that the annual aquatic emerging dry mass (DM) of these groups varied from 1.4-7.5 g m-2 yr-1, depending on the stream. We used a Bayesian approach to estimate parameters of the terrestrial dispersal function of each group. We combined emerging DM and the dispersal parameters to estimate how terrestrial deposition of aquatic insect DM varied with increasing distance from streams. The results highlighted that emerging DM and dispersal to land could be higher in intensive agricultural landscapes than that previously described in natural settings. We estimated that 12.5 kg ha-1 yr-1 of winged aquatic insect DM fell to the ground 0-10 m from stream edges, composed mainly of Ephemeroptera and Trichoptera. We also estimated that 2.2 kg DM ha-1 yr-1 fell 10-50 m from the stream, especially small-bodied species of Chironomidae, throughout the year, except for the coldest weeks of winter. By influencing aquatic insect communities that emerge from streams, intensive agricultural practices change the magnitude and spatial extent of aquatic subsidy deposition on land. Implications for terrestrial food webs and ecosystem services provided to agriculture are discussed.

Global Warming Could Magnify Insect-Driven Apparent Competition Between Native and Introduced Host Plants in Sub-Antarctic Islands.

Pristine sub-Antarctic islands terrestrial ecosystems, including many endemic species, are highly threatened by human-induced cosmopolitan plant invasion. We propose that native plant suppression could be further facilitated by the subsequent invasion by generalist pest species that could exacerbate their competitive exclusion through the process of apparent competition. By comparing the biological parameters of an invasive aphid species, Myzus ascalonicus, on one native (Acaena magellanica) and one invasive (Senecio vulgaris) plant species, we showed that survival and fecundity were higher and development time lower on the native plant species than on the invasive one. Moreover, comparing the effect of a temperature increase on the population dynamics of M. ascalonicus on the two plants, we showed that the relative profitability of the native species is further amplified by warming. Hence, while pest population doubling time is 28% higher on the invasive plant under current temperature, it would become 40% higher with an increase in temperature of 3°C. Consequently, our findings demonstrate that global warming could exacerbate competitive exclusion of native plants by invasive plants in sub-Antarctic islands by its indirect effect on the apparent competition mediated by generalist phytophagous pests.

"Generalist" Aphid Parasitoids Behave as Specialists at the Agroecosystem Scale.

The degree of trophic specialization of interacting organisms impacts on the structure of ecological networks and has consequences for the regulation of crop pests. However, it remains difficult to assess in the case of parasitoids. Host ranges are often established by listing host records from various years and geographic areas in the literature. Here, we compared the actual hosts exploited at a local farm-scale by aphid parasitoids (Hymenoptera: Aphidiinae), to the available species listed as hosts for each parasitoid species. We sampled aphids and their parasitoids in cultivated and uncultivated areas in an experimental farm from April to November 2014 and thereafter used DNA-based data to determine whether a differentiation in sequences existed. Twenty-nine parasitoid species were found on 47 potential aphid hosts. Our results showed that the great majority of the parasitoid tested used fewer host species than expected according to data published in the literature and parasitized a limited number of hosts even when other potential hosts were available in the environment. Moreover, individuals of the most generalist species differed in their DNA sequences, according to the aphid species and/or the host plant species. At a local scale, only obligate or facultative specialist aphid parasitoids were detected. Local specialization has to be considered when implementing the use of such parasitoids in pest regulation within agroecosystems.

Seasonal and spatial variations of stream insect emergence in an intensive agricultural landscape.

A growing amount of literature exists on reciprocal fluxes of matter and energy between ecosystems. Aquatic subsidies of winged aquatic insects can affect terrestrial ecosystems significantly, but this issue is rarely addressed in agroecosystems. By altering the production of benthic macroinvertebrates, agricultural practices could increase or decrease the strength of aquatic subsidies and subsequently the provision of several ecosystem services to agriculture. Effects of seasons and environmental variables on aquatic insect emergence were investigated in third-order agricultural streams in northwestern France. Most emerging dry mass (DM) of caught insects belonged to Trichoptera (56%), Chironomidae (25%) and Ephemeroptera (19%). We estimated that annual emerging dry mass of aquatic insects ranged between 1445 and 7374 mg/m2/y depending on the stream. Seasonal variations were taxon-specific, with Ephemeroptera emerging only in spring, Trichoptera emerging in spring and early summer, and Chironomidae emerging throughout the year. The percentage of watershed area covered by agriculture, ammonium concentration and hypoxia positively influenced emerging DM of Chironomidae but negatively influenced Ephemeroptera. Emerging DM of Trichoptera and Ephemeroptera increased significantly as water conductivity and temperature increased. Channel openness increased the emerging DM of all taxonomic groups, but Chironomidae were more abundant in narrow, incised streams. Assuming that the biomass of aquatic invertebrates ultimately disperse toward terrestrial habitats, nutrient accumulations on land near streams were estimated to reach 0.5-2.3 kg C ha-1 y-1, 0.1-0.5 kg N ha-1 y-1 and 0.005-0.03 kg P ha-1 y-1, depending on the stream. This suggests a significant flux of aquatic nutrients to agroecosystems and the need for future studies of its potential influence on the ecosystem services provided to agriculture.

Comparing three types of dietary samples for prey DNA decay in an insect generalist predator.

The rapidly growing field of molecular diet analysis is becoming increasingly popular among ecologists, especially when investigating methodologically challenging groups, such as invertebrate generalist predators. Prey DNA detection success is known to be affected by multiple factors; however, the type of dietary sample has rarely been considered. Here, we address this knowledge gap by comparing prey DNA detection success from three types of dietary samples. In a controlled feeding experiment, using the carabid beetle Pterostichus melanarius as a model predator, we collected regurgitates, faeces and whole consumers (including their gut contents) at different time points postfeeding. All dietary samples were analysed using multiplex PCR, targeting three different length DNA fragments (128, 332 and 612 bp). Our results show that both the type of dietary sample and the size of the DNA fragment contribute to a significant part of the variation found in the detectability of prey DNA. Specifically, we observed that in both regurgitates and whole consumers, prey DNA was detectable significantly longer for all fragment sizes than for faeces. Based on these observations, we conclude that prey DNA detected from regurgitates and whole consumers DNA extracts are comparable, whereas prey DNA detected from faeces, though still sufficiently reliable for ecological studies, will not be directly comparable to the former. Therefore, regurgitates and faeces constitute a useful, nonlethal source for dietary information that could be applied to field studies in situations when invertebrate predators should not be killed.

Impact of Agroecological Infrastructures on the Dynamics of Dysaphis plantaginea (Hemiptera: Aphididae) and Its Natural Enemies in Apple Orchards in Northwestern France.

Apple orchard production is facing new environmental and societal challenges, resulting, in particular, in strong pressure to reduce pesticide use. Cider-apple production, for which the perfect visual aspect of fruits is not a marketability imperative, offers good opportunities to study production systems that are developing new agronomic strategies, which could be subsequently extended to all apple-production types. Agroecological infrastructures play an important role in providing shelter, food resources, or reproduction habitats to many arthropods. Consequently, setting-up agroecological infrastructures in the vicinity of or within orchards could increase natural enemy presence and thus improve the biological control of pests. In this study, we focused on Dysaphis plantaginea (Passerini), one of the major pests in apple orchards in Europe, which causes important economic production losses. During two years (2014 and 2015), we monitored the population dynamics of D. plantaginea, its natural enemies, and mutualistic ants in commercial production cider-apple orchards. The influences of the cider-apple cultivar, insecticide use, and distance to agroecological infrastructures (hedgerows and flower strips) were assessed. Our results suggest that flower strips favor an increase in natural enemy abundance in the vicinity of the orchards and could thus play an important role in the production system by improving the biological control of D. plantaginea.

Larval hitch-hiking and adult flight are two ways of aphidiinae parasitoids long-range dispersal.

Dispersal strategies and success of pests' natural enemies widely influence the efficiency of biological control. In this study, we compare two dispersal strategies among Aphidiinae parasitoids: eggs and larvae dispersal through winged aphid flight and active dispersal by adult parasitoids. Using a molecular method applied to a sample of >2,000 winged migratory aphids captured in a suction trap situated in Western France, we assessed the proportion of winged aphids carrying an aphidiine larva. In the six most abundant aphid species, we found an average parasitism rate of migrating aphids close to 1% and identified seven different, mainly generalist, parasitoid species. We also identified the species and the sex of adult Aphidiinae captured by the suction trap based on morphological criteria. We found that dispersing adult parasitoids were almost exclusively female. Parasitoid dispersal strategy seems to be species-dependant but this result needs to be confirmed by an exhaustive analysis of winged aphids captured. We discuss the possible impact of the low parasitism rate of winged aphids on parasitoid population dynamics and the importance of these results in the context of biological control and of the study of food webs between aphids and their natural enemies.

Molecular analysis reveals high compartmentalization in aphid-primary parasitoid networks and low parasitoid sharing between crop and noncrop habitats.

The ecosystem service of insect pest regulation by natural enemies, such as primary parasitoids, may be enhanced by the presence of uncultivated, semi-natural habitats within agro-ecosystems, although quantifying such host-parasitoid interactions is difficult. Here, we use rRNA 16S gene sequencing to assess both the level of parasitism by Aphidiinae primary parasitoids and parasitoid identity on a large sample of aphids collected in cultivated and uncultivated agricultural habitats in Western France. We used these data to construct ecological networks to assess the level of compartmentalization between aphid and parasitoid food webs of cultivated and uncultivated habitats. We evaluated the extent to which uncultivated margins provided a resource for parasitoids shared between pest and nonpest aphids. We compared the observed quantitative ecological network described by our molecular approach to an empirical qualitative network based on aphid-parasitoid interactions from traditional rearing data found in the literature. We found that the molecular network was highly compartmentalized and that parasitoid sharing is relatively rare between aphids, especially between crop and noncrop compartments. Moreover, the few cases of putative shared generalist parasitoids were questionable and could be due to the lack of discrimination of cryptic species or from intraspecific host specialization. Our results suggest that apparent competition mediated by Aphidiinae parasitoids is probably rare in agricultural areas and that the contribution of field margins as a source of these biocontrol agents is much more limited than expected. Further large-scale (spatial and temporal) studies on other crops and noncrop habitats are needed to confirm this.

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.

A universal method for the detection and identification of Aphidiinae parasitoids within their aphid hosts.

Molecular methods are increasingly used to detect and identify parasites in their hosts. However, existing methods are generally not appropriate for studying complex host-parasite interactions because they require prior knowledge of species composition. DNA barcoding is a molecular method that allows identifying species using DNA sequences as an identification key. We used DNA amplification with primers common to aphid parasitoids and sequencing of the amplified fragment to detect and identify parasitoids in their hosts, without prior knowledge on the species potentially present. To implement this approach, we developed a method based on 16S rRNA mitochondrial gene and LWRh nuclear gene. First, we designed two primer pairs specific to Aphidiinae (Hymenoptera), the main group of aphid parasitoids. Second, we tested whether the amplified regions could correctly identify Aphidiinae species and found that 61 species were accurately identified of 75 tested. We then determined the ability of each primer pair to detect immature parasitoids inside their aphid host. Detection was earlier for 16S than for LWRh, with parasitoids detected, respectively, 24 and 48 h after egg injection. Finally, we applied this method to assess parasitism rate in field populations of several aphid species. The interest of this tool for analysing aphid-parasitoid food webs is discussed.

Identification of molecular markers for DNA barcoding in the Aphidiinae (Hym. Braconidae).

Reliable identification of Aphidiinae species (Braconidae) is a prerequisite for conducting studies on aphid-parasitoid interactions at the community level. However, morphological identification of Aphidiinae species remains problematic even for specialists and is almost impossible with larval stages. Here, we compared the efficiency of two molecular markers [mitochondrial cytochrome c oxydase I (COI) and nuclear long wavelength rhodopsin (LWRh)] that could be used to accurately identify about 50 species of Aphidiinae that commonly occur in aphid-parasitoid networks in northwestern Europe. We first identified species on a morphological basis and then assessed the consistency of genetic and morphological data. Probably because of mitochondrial introgression, Aphidius ervi and A. microlophii were indistinguishable on the basis of their COI sequences, whereas LWRh sequences discriminated these species. Conversely, because of its lower variability, LWRh failed to discriminate two pairs of species (Aphidius aquilus, Aphidius salicis, Lysiphlebus confusus and Lysiphlebus fabarum). Our study showed that no unique locus but a combination of two genes should be used to accurately identify members of Aphidiinae.

Evolutionary history of aphid-plant associations and their role in aphid diversification.

Aphids are intimately linked with their host plants that constitute their only food resource and habitat, and thus impose considerable selective pressure on their evolution. It is therefore commonly assumed that host plants have greatly influenced the diversification of aphids. Here, we review what is known about the role of host plant association on aphid speciation by examining both macroevolutionary and population-level studies. Phylogenetic studies conducted at different taxonomic levels show that, as in many phytophagous insect groups, the radiation of angiosperms has probably favoured the major Tertiary diversification of aphids. These studies also highlight many aphid lineages constrained to sets of related host plants, suggesting strong evolutionary commitment in aphids' host plant choice, but they fail to document cospeciation events between aphid and host lineages. Instead, phylogenies of several aphid genera reveal that divergence events are often accompanied by host shifts, and suggest, without constituting a formal demonstration, that aphid speciation could be a consequence of adaptation to new hosts. Experimental and field studies below the species level support reproductive isolation between host races as partly due to divergent selection by their host plants. Selected traits are mainly feeding performances and life cycle adaptations to plant phenology. Combined with behavioural preference for favourable host species, these divergent adaptations can induce pre- and post-zygotic barriers between host-specialized aphid populations. However, the hypothesis of host-driven speciation is seldom tested formally and must be weighed against overlooked explanations involving geographic isolation and non-ecological reproductive barriers in the process of speciation.

Evolution of trade-offs between sexual and asexual phases and the role of reproductive plasticity in the genetic architecture of aphid life histories.

Life-history theory postulates that evolution is constrained by trade-offs (i.e., negative genetic correlations) among traits that contribute to fitness. However, in organisms with complex life cycles, trade-offs may drastically differ between phases, putatively leading to different evolutionary trajectories. Here, we tested this possibility by examining changes in life-history traits in an aphid species that alternates asexual and sexual reproduction in its life cycle. The quantitative genetics of reproductive and dispersal traits was studied in 23 lineages (genotypes) of the bird cherry-oat aphid Rhopalosiphum padi, during both the sexual and asexual phases, which were induced experimentally under specific environmental conditions. We found large and significant heritabilities (broad-sense) for all traits and several negative genetic correlations between traits (trade-offs), which are related to reproduction (i.e., numbers of the various sexual or asexual morphs) or dispersal (i.e., numbers of winged or wingless morphs). These results suggest that R. padi exhibits lineage specialization both in reproductive and dispersal strategies. In addition, we found important differences in the structure of genetic variance-covariance matrices (G) between phases. These differences were due to two large, negative genetic correlations detected during the asexual phase only: (1) between fecundity and age at maturity and (2) between the production of wingless and winged parthenogenetic females. We propose that this differential expression in genetic architecture results from a reallocation scheme during the asexual phase, when sexual morphs are not produced. We also found significant G x E interaction and nonsignificant genetic correlations across phases, indicating that genotypes could respond independently to selection in each phase. Our results reveal a rather unique situation in which the same population and even the same genotypes express different genetic (co)variation under different environmental conditions, driven by optimal resource allocation criteria.

A continuum of genetic divergence from sympatric host races to species in the pea aphid complex.

Sympatric populations of insects adapted to different host plants, i.e., host races, are good models to investigate how natural selection can promote speciation in the face of ongoing gene flow. However, host races are documented in very few model systems and their gradual evolution into good species, as assumed under a Darwinian view of species formation, lacks strong empirical support. We aim at resolving this uncertainty by investigating host specialization and gene flow among populations of the pea aphid complex, Acyrthosiphon pisum. Genetic markers and tests of host plant specificity indicate the existence of at least 11 well-distinguished sympatric populations associated with different host plants in Western Europe. Population assignment tests show variable migration and hybridization rates among sympatric populations, delineating 8 host races and 3 possible species. Notably, hybridization correlates negatively with genetic differentiation, forming a continuum of population divergence toward virtually complete speciation. The pea aphid complex thus illustrates how ecological divergence can be sustained among many hybridizing populations and how insect host races blend into species by gradual reduction of gene flow.

Landscape epidemiology of plant diseases.

Many agricultural landscapes are characterized by a high degree of heterogeneity and fragmentation. Landscape ecology focuses on the influence of habitat heterogeneity in space and time on ecological processes. Landscape epidemiology aims at applying concepts and approaches originating from landscape ecology to the study of pathogen dynamics at the landscape scale. However, despite the strong influence that the landscape properties may have on the spread of plant diseases, landscape epidemiology has still received little attention from plant pathologists. Some recent methodological and technological progress provides new and powerful tools to describe and analyse the spatial patterns of host-pathogen interactions. Here, we review some important topics in plant pathology that may benefit from a landscape perspective. These include the influence of: landscape composition on the global inoculum pressure; landscape heterogeneity on pathogen dynamics; landscape structure on pathogen dispersal; and landscape properties on the emergence of pathogens and on their evolution.

Temporal habitat variability and the maintenance of sex in host populations of the pea aphid.

The evolutionary maintenance of sex, despite competition from asexual reproduction, has long intrigued the evolutionary biologists owing to its numerous apparent short-term costs. In aphids, winter climate is expected to determine the maintenance of sexual lineages in the high latitude zones owing to their exclusive ability to produce frost-resistant eggs. However, diverse reproductive modes may coexist at a local scale where climatic influence is counteracted by microgeographical factors. In this study, we tested the influence of local habitat characteristics on regional coexistence of reproductive modes in the pea aphid, Acyrthosiphon pisum. In the laboratory, the induction of sexual morph production of many pea aphid genotypes from the local fields of annual (pea and faba bean) and perennial (alfalfa and red clover) crops in Western France indicated that A. pisum lineages from annual crops had a significantly higher investment in sexual reproduction than A. pisum lineages from the perennial hosts. We propose that temporal habitat variability exerts a selective pressure to maintain the sexual reproduction in A. pisum. The ecological and evolutionary consequences of the association between the mode of reproduction and the host population on gene flow restriction and on ecological specialization are discussed.

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.