Local pesticide use intensity conditions landscape effects on biological pest control.

Complex landscapes including semi-natural habitats are expected to favour natural enemies thereby enhancing natural pest biocontrol in crops. However, when considering a large number of situations, the response of natural biocontrol to landscape properties is globally inconsistent, a possible explanation being that local agricultural practices counteract landscape effects. In this study, along a crossed gradient of pesticide use intensity and landscape simplification, we analysed the interactive effects of landscape characteristics and local pesticide use intensity on natural biocontrol. During 3 years, using a set of sentinel prey (weed seeds, aphids and Lepidoptera eggs), biocontrol was estimated in 80 commercial fields located in four contrasted regions in France. For all types of prey excepted weed seeds, the predation rate was influenced by interactions between landscape characteristics and local pesticide use intensity. Proportion of meadow and length of interface between woods and crops had a positive effect on biocontrol of aphids where local pesticide use intensity was low but had a negative effect elsewhere. Moreover, the landscape proportion of suitable habitats for crop pests decreased the predation of sentinel prey, irrespectively of the local pesticide use intensity for weed seeds, but only in fields with low pesticide use for Lepidoptera eggs. These results show that high local pesticide use can counteract the positive expected effects of semi-natural habitats, but also that the necessary pesticide use reduction should be associated with semi-natural habitat enhancement to guarantee an effective natural biocontrol.

Ecological specialization in Diaeretiella rapae (Hymenoptera: Braconidae: Aphidiinae) on aphid species from wild and cultivated plants.

Diaeretiella rapae is an aphid parasitoid with potential for use in biological control strategies. However, several recent genetic studies have challenged the long held view that it is a generalist parasitoid. We investigated its ecological specialization and ability to use resources in cultivated and uncultivated areas. Ecological specialization would reduce its ability to exploit the diversity of aphid species, particularly in uncultivated areas, and to control pest aphids. Four D. rapae strains were studied, three reared on pest aphids on Brassicaceae and one strain on a non-pest aphid on Chenopodiaceae. For each strain, we performed host-switching experiments, with a total of six aphid species, five of which D. rapae parasitizes in France. We tested cross-breeding ability between strains to detect potential reproductive isolation linked to aphid host species in D. rapae. The strain reared on non-pest aphids was able to develop on aphid species from both cultivated and uncultivated plants. The strains reared on pest aphids, however, exclusively parasitized aphid species on cultivated Brassicaceae. In addition, reproductive isolation was detected between strains from uncultivated and cultivated plants. Thus, the D. rapae populations examined here appear to be showing ecological specialization or they may even be composed of a complex of cryptic species related to the aphid hosts. The role of Chenopodium album as a reservoir for D. rapae, by providing a habitat for non-pest aphids on which it can feed, appears to be severely limited, and thus its efficiency to maintain local populations of D. rapae in the vicinity of crops is questionable.

Community-wide stable isotope analysis reveals two distinct trophic groups in a service-providing carabid community.

Disentangling trophic interactions among species is important for elucidating mechanisms underlying ecosystem functioning and services. Carabid beetles are an important guild of predators that may regulate pest populations in arable landscapes, but their generalist feeding behavior hinders predictions about their actual contribution to pest control. In order to assess carabids' potential for pest control, we simultaneously analyzed the carbon and nitrogen stable isotope ratios of a community of 45 co-occurring species in wheat and oilseed rape fields. With the expectation to identify distinct trophic groups based on the mean and the variance of carabid isotopic signatures, we observed a high degree of overlap in trophic positions between species. However, we also observed that species could be successfully categorized into two groups according to whether or not their carbon signatures varied independently from variations in the crop baseline. We interpret these results as differential primary resource uptake or by differential mobility aptitude in foraging. Accordingly, we propose that the isotopic signal can inform us on the presence/absence of links between generalist predators and cultivated plants through the trophic networks they belong to, and consequently on their potential role as pest natural enemies. We therefore suggest the complementarity of stable isotope analysis for obtaining a time-integrated assessment of carabid trophic behavior that may be combined with more direct molecular diet analysis allowing the simultaneous quantification of specific trophic links within agricultural landscapes.

Longitudinal clines in the frequency distribution of 'super-clones' in an aphid crop pest.

Parthenogenesis is the main mode of reproduction of aphids. Their populations are therefore composed of clones whose frequency distribution varies in space and time. Previous population genetic studies on aphids have highlighted the existence of highly abundant clones ('super-clones'), distributed over large geographic areas and persisting over time. Whether the abundance of 'super-clones' results from their ecological success or from stochastic forces, such as drift and migration, is an open question. Here, we looked for the existence of clines in clonal frequency along a climatic gradient in the cereal aphid Rhopalosiphum padi (Linnaeus, 1758) and examined the possible influence of geographical distance and environmental variables in the buildup and maintenance of such clonal clines. We investigated the spatial distribution of the commonest genotypes of R. padi by sampling populations along an east-west transect in maize fields in the northern half of France in both spring and late summer. Individual aphids were genotyped at several polymorphic loci, allowing the assessment of frequency distributions of multilocus genotypes (MLGs) across the cropping season. We found several MLGs showing longitudinal clines in their frequency distribution in both spring and summer. In particular, two dominant asexual genotypes of R. padi showed inverted geographical clines, which could suggest divergent adaptations to environmental conditions. We concluded that while the distribution of some 'super-clones' of R. padi seems most likely driven by the action of migration and genetic drift, selection could be also involved in the establishment of longitudinal clines of others.

Host races of the pea aphid Acyrthosiphon pisum differ in male wing phenotypes.

The evolution of reproductive isolation without geographic isolation (sympatric speciation) has recently gained strong theoretical and empirical supports. It is now widely admitted that many host-specific phytophagous insect species have arisen through shifting and adapting to new plants. The pea aphid Acyrthosiphon pisum has received considerable attention in this context and is now considered as a probable case of incipient sympatric speciation through host specialization. In Europe, three host races have been described so far, one on annual plants (pea and broad bean) and two on perennial plants (red clover and alfalfa, respectively). These host races are genetically differentiated and exhibit strong ecological specialization affecting their preferences and performances on alternative plants. Here, we investigate whether other life-history traits of ecological importance are associated with host specialization in the species. In particular, because A. pisum shows a genetically determined male wing variation, we tested if its host races also differ in their proportion of winged/wingless male phenotypes. We used a large collection of pea aphid lineages sampled on pea, broad bean, red clover and alfalfa and analyzed their male production by placing them in conditions inducing the sexual phase in A. pisum. Striking differences in the frequency of male dispersal genotypes were found between host populations; aphids producing winged males were in high proportion among lineages from annual hosts, while those producing wingless males were in high proportion on perennial ones. The evolutionary maintenance and ecological consequences of this association between habitat specialization and male wing variation are discussed.

Climate and agricultural context shape reproductive mode variation in an aphid crop pest.

In aphids, reproductive mode is generally assumed to be selected for by winter climate. Sexual lineages produce frost-resistant eggs, conferring an advantage in regions with cold winters, while asexual lineages predominate in regions with mild winters. However, habitat and resource heterogeneities are known to exert a strong influence on sex maintenance and might modulate the effect of climate on aphid reproductive strategies. We carried out a hierarchical sampling in northern France to investigate whether reproductive mode variation of the aphid Rhopalosiphum padi is driven by winter climate conditions, by habitat and resource heterogeneities represented by a range of host plants or by both factors. We confirmed the coexistence in R. padi populations of two genetic clusters associated with distinct reproductive strategies. Asexual lineages predominated, whatever the surveyed year and location. However, we detected a between-year variation in the local contribution of both clusters, presumably associated with preceding winter severity. No evidence for host-driven niche differentiation was found in the field on six Poaceae among sexual and asexual lineages. Two dominant multilocus genotypes ( approximately 70% of the sample), having persisted over a 10-year period, were equally abundant on different plant species and locations, indicating their large ecological tolerance. Our results fit theoretical predictions of the influence of winter climate on the balance between sexual and asexual lineages. They also highlight the importance of current agricultural practices which seem to favour a small number of asexual generalist genotypes and their migration across large areas of monotonous environments.

Gene flow between sexual and facultatively asexual lineages of an aphid species and the maintenance of reproductive mode variation.

Many organisms considered as strictly clonal may in fact experience some rare events of sexual reproduction with their sexual relatives. However, the rate of sexual-asexual gene flow has rarely been assessed mainly because its evaluation is difficult to achieve in the field. In the cyclically parthenogenetic aphid Rhopalosiphum padi, two main sets of lineages, differing in their investment in sexual reproduction and in their genetic attributes, co-exist even at a very fine scale: the 'sexual' lineages which have a full commitment to the sexual reproduction, and the 'facultatively asexual' lineages, which allocate investment in the sexual and parthenogenetic reproduction. This system offers a unique opportunity to tackle the genetic interactions between two contrasting reproductive modes. Here, we provide evidence that gene flow occurred between sexual and facultatively asexual lineages of R. padi. We carefully examined the shuffling in phenotypic and genotypic variation following a sexual reproduction event that took place in the field. Combining genotypic data and phenotypic measurements showed that this gene mixing led to the production of a wide array of reproductive modes, including strictly asexual lineages. Finally, we discuss the central role played by facultatively asexual lineages on the maintenance of reproductive mode variation.

Short-term population differences in the genetic architecture of life history traits related to sexuality in an aphid species.

One of the most important factors that determine the evolutionary trajectory of a suite of traits in a population is the structure of the genetic variance-covariance matrix (G). We studied the cyclically parthenogenetic aphid Rhopalosiphum padi, whose populations exhibit two types of reproductive lineages respectively specialized in sexuality (that is, cyclically parthenogenetic lineages) and in asexuality (that is, obligate parthenogenetic lineages). We compared the quantitative genetics of life histories in these two lineage types. Our results suggest that both, the elements and the whole structure of the resulting G matrices differ in the very short term, between lineage types. This would involve the evolution toward different evolutionary optima in the same population, depending on whether sexual or asexual lineages predominate. Since sexual and asexual lineages vary seasonally in their abundance, a fluctuating selective regime has been proposed for this species, which would contribute to the maintenance of the reproductive polymorphism that these populations exhibit.

Host range expansion of an introduced insect pest through multiple colonizations of specialized clones.

Asexuality confers demographic advantages to invasive taxa, but generally limits adaptive potential for colonizing of new habitats. Therefore, pre-existing adaptations and habitat tolerance are essential in the success of asexual invaders. We investigated these key factors of invasiveness by assessing reproductive modes and host-plant adaptations in the pea aphid, Acyrthosiphon pisum, a pest recently introduced into Chile. The pea aphid encompasses lineages differing in their reproductive mode, ranging from obligatory cyclical parthenogenesis to fully asexual reproduction. This species also shows variation in host use, with distinct biotypes specialized on different species of legumes as well as more polyphagous populations. In central Chile, microsatellite genotyping of pea aphids sampled on five crops and wild legumes revealed three main clonal genotypes, which showed striking associations with particular host plants rather than sampling locations. Phenotypic analyses confirmed their strong host specialization and demonstrated parthenogenesis as their sole reproductive mode. The genetic relatedness of these clonal genotypes with corresponding host-specialized populations from the Old World indicated that each clone descended from a particular Eurasian biotype, which involved at least three successful introduction events followed by spread on different crops. This study illustrates that multiple introductions of highly specialized clones, rather than local evolution in resource use and/or selection of generalist genotypes, can explain the demographic success of a strictly asexual invader.

Financial benefit of using crop protection decision rules over systematic spraying strategies.

ABSTRACT Decision rule models are considered to be one of the main cornerstones of the implementation of integrated pest management (IPM) programs. Even if the need for such programs to offer cost advantages over conventional strategies is a major incentive for IPM adoption, few studies focus on this financial dimension. In this article, a modeling approach of the response of a pathosystem to a disease control method and of the predictive performance of decision rules is used to explore how some basic factors act on the likelihood of adoption of decision rule models strategies (such as using an IPM system) over systematic strategies (such as systematic-spraying and never-spraying strategies). Even if the average cost of using the decision rule strategies is always lower than the average cost of systematic strategies in several different scenarios, the models developed here showed strong effects of different pathosystems and decision rules on financial benefits. The number of production situations where decision rules are of interest is highly correlated with their accuracy. However, because of the inescapable trade-offs between decision rule accuracy and limiting factors such as its user-friendly characteristics, the use of decision rules is unlikely to reduce costs to <70% of the costs of systemic strategies. In more general terms, this study provides quantitative guidelines on the financial advantage that decision rules can offer in plant protection as well as a better understanding of their potential usefulness.

Temporal differentiation and spatial coexistence of sexual and facultative asexual lineages of an aphid species at mating sites.

Cases of coexisting sexual and asexual relatives are puzzling, as evolutionary theory predicts that competition for the same ecological niches should lead to the exclusion of one or the other population. In the cyclically parthenogenetic aphid, Rhopalosiphum padi, sexual and facultative asexual lineages are admixed in space at the time of sexual reproduction. We investigated how the interaction of reproductive mode and environment can lead to temporal niche differentiation. We demonstrated theoretically that differential sensitivity of sexual and facultatively asexual aphids to an environmental parameter (mating host suitability) shapes the two strategies: whereas the sexual lineages switch earlier to the production of sexual forms, the facultative asexual lineages delay and spread out their investment in sexual reproduction. This predicted pattern of niche specialization is in agreement with the temporal structure revealed in natura by demographic and genetic data. We propose that partial loss of sex by one pool of aphids and subsequent reduction in gene flow between lineages may favour temporal specialization through disruptive selection.

Ecological specialization correlates with genotypic differentiation in sympatric host-populations of the pea aphid.

The pea aphid, Acyrthosiphon pisum, encompasses distinct host races specialized on various Fabaceae species, but the extent of genetic divergence associated with ecological specialization varies greatly depending on plant and geographic origins of aphid populations. Here, we studied the genetic structure of French sympatric pea aphid populations collected on perennial (pea and faba bean) and annual (alfalfa and red clover) hosts using 14 microsatellite loci. Classical and Bayesian population genetics analyses consistently identified genetic clusters mostly related to plant origin: the pea/faba bean cluster was highly divergent from the red clover and the alfalfa ones, indicating they represent different stages along the continuum of genetic differentiation. Some genotypes were assigned to a cluster differing from the one expected from their plant origin while others exhibited intermediate genetic characteristics. These results suggest incomplete barriers to gene flow. However, this limited gene flow seems insufficient to prevent ecological specialization and genetic differentiation in sympatry.

Admixed sexual and facultatively asexual aphid lineages at mating sites.

Cyclically parthenogenetic organisms may have facultative asexual counterparts. Such organisms, including aphids, are therefore interesting models for the study of ecological and genetic interactions between lineages differing in reproductive mode. Earlier studies on aphids have revealed major differences in the genetic outcomes of populations that are possibly resulting mostly either from sexual or from asexual reproduction. Besides, notable gene flow between sexual and asexual derivatives has been suspected, which could lead to the emergence of new asexual lineages. The present study examines the interplay between these lineages and is based on analyses of population structure of individuals that may contribute to the pool of sexual reproductive forms in the host alternating aphid Rhopalosiphum padi. Using a Bayesian assignment method, we first show that the sexual forms of R. padi on mating sites encompass two genetically distinct clusters of individuals in the western part of France. The first cluster included unique genotypes of sexual lineages, while the second cluster included facultatively asexual lineages in numerous copies, the reproductive mode of the two clusters being confirmed by reference clones. Sexual reproductive forms produced by sexual and facultatively asexual lineages are thus admixed at mating sites which gives a large opportunity for the two clusters to mate with each other. Nevertheless, this study also highlights, as previously demonstrated, that the two clusters retained high genetic differentiation. Possible explanations for the inferred limited genetic exchanges are advanced in the discussion, but further dedicated investigations are required to solve this paradox.

Aphid Abundance on Cereals in Autumn Predicts Yield Losses Caused by Barley yellow dwarf virus.

ABSTRACT Barley yellow dwarf virus (BYDV) damage to winter cereals and population dynamics of the aphid Rhopalosiphum padi during fall were monitored in fields during 10 years at various locations in the northern half of France. Logistic regression was used to examine whether a simple risk probability algorithm based only on the autumnal population dynamics of R. padi can accurately predict yield losses caused by BYDV and, therefore, the need for insecticide treatment. Results showed that the area under the curve of the percentage of plants infested by R. padi during autumn was highly significantly related to BYDV yield losses. Then, a cost/benefit analysis was performed to estimate the optimal decision threshold resulting in the lowest annual average costs of BYDV damage and control. A "model use" strategy allowed a reduction in the annual average costs of BYDV disease and control of up to 36% when compared with a "prophylactic spraying" strategy. The optimal decision threshold was highly sensitive to variation in disease prevalence. This property was used to propose an easy way to adapt the model to any production situation through the determination of the most accurate decision threshold.

Superparasitism limitation in an aphid parasitoid: cornicle secretion avoidance and host discrimination ability.

Superparasitism avoidance by the endoparasitoid Aphidius rhopalosiphi De Stefani Perez on the grain aphid, Sitobion avenae was studied. Experiments were carried out in which aphids were exposed to two consecutive attacks by parasitoids. Results showed that superparasitism avoidance in A. rhopalosiphi was mediated by two successive stimuli whose effectiveness depended on the time interval between attacks. For short time intervals (<16 h), host rejections were mainly associated with the presence of dried cornicle secretion on the host's body which was exuded during the first attack. The repellency of this secretion declined with the time interval between attacks, becoming ineffective 2 days after the first parasitization, and allowed females to reject up to 30% of parasitized hosts. For longer time intervals (>/=16 h), host rejection behavior was a response of parasitoid females to internal changes in host quality associated with parasite development. This response gradually increased with an increase in time interval, reaching no more than 60%, 96 h after initial parasitization. This host discrimination ability did not allow females to distinguish between hosts parasitized by themselves or by conspecifics. Consequently, these findings suggest that superparasitism is a common event in A. rhopalosiphi and especially on recently parasitized hosts.

Evidence for predominant clones in a cyclically parthenogenetic organism provided by combined demographic and genetic analyses.

Aphids are particularly interesting models in the study of genetic and demographic components of plant adaptation because of their breeding system which combines parthenogenesis and sexual reproduction (i.e. cyclical parthenogenesis), and the frequent emergence of host-adapted races reported in this group. In this paper, patterns of host adaptation were assessed on local populations of the aphid Sitobion avenae by following their demographic and genetic structure in a maize field for two consecutive years. The existence of putative generalist (polyphagous) or specialized (host-adapted) genotypes was also investigated by comparing the genotypic distribution of this aphid on maize and other cultivated host plants, using five microsatellite loci. Although population dynamics revealed strong variation in aphid abundance during the colonization period on maize, two genotypes identified at seven additional microsatellite loci were predominant and exhibited stable frequencies over cropping season and between years. Based on present and earlier studies, these two prevalent genotypes were shown to survive on different host plants other than maize, to colonize large geographical zones and to persist parthenogenetically for several years. All these data strongly suggest that these two genotypes are asexual generalist clones that could have been favoured by agricultural practices encountered in western Europe. Besides these two clones, a continual replacement of rare genotypes was observed on maize in both years. Hypotheses involving selection via aphid-plant interactions and natural enemies were proposed for explaining the disappearance of these genotypes on maize.

Analyzing and Modeling Temporal Disease Progress of Barley yellow dwarf virus Serotypes in Barley Fields.

ABSTRACT Population dynamics of Padi avenae (PAV), Macrosiphum avenae (MAV), and Rhopalosiphum padi (RPV) virus serotypes of Barley yellow dwarf virus (BYDV) and of their main aphid vectors were studied in winter barley (Hordeum vulgare) fields for three successive years in western France. An epidemiological model of the spread of viruses in the field was developed based on vector populations as forcing variables and the population dynamics of each virus serotype. This model accurately simulated the kinetics of the epidemic for PAV serotypes, which are the most common ones. For RPV and to some extent for MAV, the results were less satisfactory. The occurrence and spread of PAV and MAV serotypes in the field was clearly and easily related to that of their main vector species. Conversely, the spread of RPV serotypes showed no consistent relationships with the dynamics of their vectors. Incidence of PAV in 1989 to 1990 and 1990 to 1991 showed a bimodal distribution, with maximums in fall (December) and spring (May) that were linked to fall infestations by R. padi and spring infestations by three (R. padi, Sitobion avenae, and Metopolophium dirhodum) or two (S. avenae and M. dirhodum) aphid species. In 1991 to 1992, the PAV infection curve was monomodal and mainly due to a primary spread of the virus by very large populations of alate R. padi. MAV incidence was low in fall and winter and reached a maximum in spring 1990 and 1991 related to the occurrence of S. avenae and M. dirhodum. RPV incidence was low every year, despite the abundance of its vector, R. padi. Mixed infections were more frequent than expected by chance and were assumed to be partly related to heterologous encapsidation. The occurrence of each serotype is discussed in relation to the time of crop infection and possible damage.