Aphid Parasitoid Community Research Articles

Aggregation of organically managed fields promotes aphid parasitism in cereal crops under Mediterranean conditions

ContextMaintaining a balance between semi-natural habitats and arable land is not always feasible for farmers. The promotion of biological control agents can be addressed through management at farm or field level, and/or by deploying lower intensity, biodiversity-friendly practices which can act either directly or indirectly through their effect of the plant community.ObjectivesWe studied the effects on cereal aphids and their parasitoids of agricultural management at field and landscape levels. We tested the effect of organic and conventional farming, and of the within field characteristics, on the cereal aphid-parasitoid community, across a gradient of organic farming aggregation and of percentage of arable land.MethodsIn spring 2015, we sampled aphid populations in 30 cereal fields in five agricultural areas in Catalonia (Spain) with contrasting levels of organic farming aggregation. In each field, we also assessed weed and crop cover. As landscape variables, we calculated the Percentage of Agricultural Land (PAL) and the Percentage of Organically Managed Land (POML) in a 500-m buffer around each field. We sampled cereal tillers 3 m from the field edges and collected all aphids detected. In addition, we reared mummies (parasitized aphids) until they hatched.ResultsOur results show that management at landscape level has significant effects on parasitism rates: a higher proportion of surrounding fields under organic management increased the amount of parasitism, as did less agricultural land cover. On the other hand, aphid populations were mainly affected by two in-field factors, namely, crop density and crop variety. Differences in weed communities did not seem to have any effects on either aphids or parasitoids.ConclusionsRather than concentrating on the individual management of fields, a coordinated implementation of organic farming at landscape level would seem to be a much better strategy for improving the biological control of aphids.

Spectrum of artificial light at night drives impact of a diurnal species in insect food web

Artificial light at night (ALAN) has become a profound form of global anthropogenic environmental change differing in from natural light regimes in intensity, duration, distribution and spectra. It is clear that ALAN impacts individual organisms, however, population level effects, particularly of spectral changes, remain poorly understood. Here we exposed experimental multigenerational aphid-parasitoid communities in the field to seven different light spectra at night ranging from 385 to 630 nm and compared responses to a natural day-night light regime. We found that while aphid population growth was initially unaffected by ALAN, parasitoid efficiency declined under most ALAN spectra, leading to reduced top-down control and higher aphid densities. These results differ from those previously found for white light, showing a strong impact on species' daytime performance. This highlights the importance of ALAN spectra when considering their environmental impact. ALAN can have large impacts on the wider ecological community by influencing diurnal species.

The impact of climate on the winter strategies of insects

The impact of climate on the winter strategies of insects

Rapid Responses of Winter Aphid-Parasitoid Communities to Climate Warming

Consequences of environmental fluctuations, including those associated with climate changes, can have a knock-on effect from individual to community scale. In particular, changes in species seasonal phenology can modify the structure and composition of communities, with potential consequences on their functioning and the provision of ecosystem services. In mild climate areas, aphids can be present in cereal fields throughout the winter, which allows aphid parasitoids to remain active. Using a nine-year dataset of aphid-parasitoid winter trophic webs in cereal fields of Western France, we report that the community structure and composition that prevailed before 2011 have recently shifted toward a more diversified community, with the presence of two new braconid parasitoid species (Aphidius ervi and Aphidius avenae), a few hyperparasitoid species and one aphid species (Metopolophium dirhodum). Increases in minimal winter temperatures and the frequency of frost events across the years partially explain observed community changes. Strong bottom-up effects from the relative abundances of aphid species also determine the relative abundance of parasitoid species each winter. Strong compartmentalization in parasitoid preference for host is reported. We suggest the recent modifications in parasitoid community composition to be linked to shifts in diapause expression (reduction or arrest of the use of winter diapause) and to host availability throughout the year. We highlight the implications for natural biological control in cereal fields. Perspectives are proposed to predict the composition of future host-parasitoid communities in the climate change context.

Shifting daylength regimes associated with range shifts alter aphid-parasitoid community dynamics.

With climate change leading to poleward range expansion of species, populations are exposed to new daylength regimes along latitudinal gradients. Daylength is a major factor affecting insect life cycles and activity patterns, so a range shift leading to new daylength regimes is likely to affect population dynamics and species interactions; however, the impact of daylength in isolation on ecological communities has not been studied so far. Here, we tested for the direct and indirect effects of two different daylengths on the dynamics of experimental multitrophic insect communities. We compared the community dynamics under “southern” summer conditions of 14.5‐hr daylight to “northern” summer conditions of 22‐hr daylight. We show that food web dynamics indeed respond to daylength with one aphid species (Acyrthosiphon pisum) reaching much lower population sizes at the northern daylength regime compared to under southern conditions. In contrast, in the same communities, another aphid species (Megoura viciae) reached higher population densities under northern conditions. This effect at the aphid level was driven by an indirect effect of daylength causing a change in competitive interaction strengths, with the different aphid species being more competitive at different daylength regimes. Additionally, increasing daylength also increased growth rates in M. viciae making it more competitive under summer long days. As such, the shift in daylength affected aphid population sizes by both direct and indirect effects, propagating through species interactions. However, contrary to expectations, parasitoids were not affected by daylength. Our results demonstrate that range expansion of whole communities due to climate change can indeed change interaction strengths between species within ecological communities with consequences for community dynamics. This study provides the first evidence of daylength affecting community dynamics, which could not be predicted from studying single species separately.

Spatiotemporal variations in aphid‐parasitoid relative abundance patterns and food webs in agricultural ecosystems

Understanding the stability of communities is fundamental in theoretical and applied ecology. Organisms atop trophic chains are particularly sensitive to disturbance, especially when they are dependent on a specific trophic resource subject to strong fluctuations in density and quality, which is the case of parasitoids. We investigated the (1) variability in spatiotemporal relative abundance patterns of a cereal aphid parasitoid community, determining at what scales such patterns vary in agrosystems. We also investigated whether (2) parasitoid relative abundances are strongly influenced by host relative abundances and if (3) different host species are exploited at distinct rates. Aphid parasitoid populations were monitored in three remote agricultural regions in France between 2010 and 2012. Five parasitoid species (Hymenoptera: Braconidae: Aphidiinae) and three aphid species (Hemiptera: Aphididae) were identified in each of those three regions. Fields sampled in one region in a single year exhibited similar relative abundance patterns, with aphid parasitoid communities varying across regions and years. All parasitoid species were able to exploit each monitored host species. Metopolophium dirhodum Wlk was consistently a more frequent species among parasitized aphids than among living aphids, indicating that this aphid species was exploited at a higher rate than the other two aphid species found (Sitobion avenae F and Rhopalosiphum padi L). Those findings suggest the cereal aphid‐parasitoid network is not strictly determined by the intrinsic permanent environmental characteristics but partially varies from one year to another. The similarity in abundance patterns in different fields of a region in a given year suggests the existence of a mechanism allowing a rapid synchronisation of the relative abundance patterns at an intra‐regional scale. This phenomenon could be useful in predicting host‐parasitoid communities and bear important consequences for the ecosystem service provided by parasitoids.

Untangling the aphid-parasitoid food web in citrus: Can hyperparasitoids disrupt biological control?

Molecular techniques are irreplaceable to untangle the trophic links in communities where immature entomophagous species (either in the third or fourth level) develop inside the phytophagous. This is the case of aphid-parasitoid communities. Here, we develop a DNA-based approach to untangle the structure of the aphid-parasitoid food web in citrus, where Aphis spiraecola Patch. (Hemiptera: Aphididae) is a key pest and Binodoxys angelicae Haliday (Hymenoptera: Braconidae), its dominant primary parasitoid, is attacked by a complex of hyperparasitoids. Aphid populations and parasitism were followed at weekly intervals in 2012 and 2013. Parasitism rates were low (∼0.04 in the four sampled orchards). Simultaneously, colonies harboring aphid mummies were collected. Approximately half of the mummies were reared to adulthood and at least six hymenopteran hyperparasitoid species were identified by classical means: Syrphophagus aphidivorus (Mayr) (Encyrtidae), Alloxysta sp. (Forster) (Figitidae), Asaphes sp. (Walker) (Pteromalidae), Pachyneuron aphidis (Bouché) (Pteromalidae), Dendrocerus sp. (Ratzeburg) (Megaspilidae) and Phaenoglyphis villosa (Hartig) (Figitidae). The other half was subjected to a Taqman-based multiplex PCR to investigate trophic relationships in this food web. We confirmed that all six species hyperparasitized B. angelicae. The most abundant hyperparasitoids were S. aphidivorus and Alloxysta sp. Both were abundant from the beginning of the season, and hyperparasitism rates remained high (∼0.4) throughout the season in the two study years. Although these species could share the same mummy, S. aphidivorus and Alloxysta sp. were the most abundant species and dominated this food web. Finally, hyperparasitoids also increased the secondary sex ratio of B. angelicae. Thus, hyperparasitism probably explains the low impact of B. angelicae on A. spiraecola populations.

The impacts of extreme and fluctuating temperatures on trait-mediated indirect aphid-parasitoid interactions

1. Global climate change models predict an increase in the frequency and magnitude of extreme temperature events. These temperature events, heatwaves for example, will impact a wide range of physiological and behavioural processes, particularly in ectotherms, and may therefore influence interactions between species. 2. Anti-predator responses may be more costly under more severe temperature regimes and therefore trait-mediated disturbance could lead to high mortality or reduced reproduction under extreme and fluctuating temperature regimes. 3. We examined the impacts of extreme and fluctuating temperatures on trait-mediated indirect interactions in an aphid–parasitoid community. 4. In treatments that isolated the effects of trait-mediated disturbance from the effects of foraging parasitoids we found that an increase in both the amplitude and frequency of peak temperatures reduced aphid numbers and provided evidence that the cost of trait-mediated disturbance could increase under frequent periods of high temperature. Aphid dispersal also increased with more frequent periods of high temperature. 5. In treatments where female wasps were allowed to freely forage (direct + trait-mediated effects), there was no evidence that extreme and fluctuating temperatures influenced the wasp's foraging ability. Exposure to extreme fluctuating temperatures did not influence the offspring production of exposed wasps or the position of the mummies within the plots.

Development and use of molecular diagnostic tools to determine trophic links and interspecific interactions in aphid–parasitoid communities in Hawaii

There has been much debate regarding the impact of parasitoid competition and hyperparasitism on the successful biological control of aphid pests. Difficulty in the evaluation of interspecific interactions and trophic links using conventional rearing and dissection methods has prevented a deeper understanding of such relationships. The analysis of trophic links in the parasitoid community associated with the melon aphid ( Aphis gossypii) in Hawaii provides a unique opportunity to assess complex interactions that occur in a system where all of the aphids and parasitoids have been introduced. Here, we developed and applied multiplex PCR assays to investigate the occurrence of in-host competition between parasitoids and/or hyperparasitoids on melon aphids collected from fields of Colocasia esculenta. To fully document the parasitoid–hyperparasitoid community within A. gossypii, both live and mummified aphids were examined. A total of 818 live and 245 mummified aphids were analyzed using the multiplex assays, with congruent rearing of over 600 mummified aphids serving as a basis for qualitative comparisons in terms of species composition and trophic linkages. The rearing and the DNA methods showed similar trends, with sharp declines in one parasitoid species followed by sharp increases in another during the course of the season. Molecular analyses revealed that hyperparasitism and multiparasitism of live aphids is remarkably low, whereas hyperparasitism of mummified aphids was extraordinarily high in both rearing and molecular analyses. In comparison to reared samples, molecular analysis of the parasitoid community was more complete and permitted the identification of previously unknown or unconfirmed trophic linkages. The potential of this approach in future studies on the biological control of aphids in Hawaii, particularly in light of new parasitoid introductions, is discussed.

Aphid–parasitoid community structure on genetically modified wheat

Since the introduction of genetically modified (GM) plants, one of the main concerns has been their potential effect on non-target insects. Many studies have looked at GM plant effects on single non-target herbivore species or on simple herbivore-natural enemy food chains. Agro-ecosystems, however, are characterized by numerous insect species which are involved in complex interactions, forming food webs. In this study, we looked at transgenic disease-resistant wheat (Triticum aestivum) and its effect on aphid-parasitoid food webs. We hypothesized that the GM of the wheat lines directly or indirectly affect aphids and that these effects cascade up to change the structure of the associated food webs. Over 2 years, we studied different experimental wheat lines under semi-field conditions. We constructed quantitative food webs to compare their properties on GM lines with the properties on corresponding non-transgenic controls. We found significant effects of the different wheat lines on insect community structure up to the fourth trophic level. However, the observed effects were inconsistent between study years and the variation between wheat varieties was as big as between GM plants and their controls. This suggests that the impact of our powdery mildew-resistant GM wheat plants on food web structure may be negligible and potential ecological effects on non-target insects limited.

Effect of plant species loss on aphid–parasitoid communities

1. The consequences of species loss on ecosystem functioning within a single trophic level have been extensively studied. However, the loss of basal species is likely to have profound impacts on the abundance, richness and ecosystem functioning of species at higher trophic levels. 2. Here, we used experimentally established plant communities with a species richness gradient to study the effects of plant species loss on a multi-trophic insect community in the field. We measured densities and species richness of aphids and parasitic wasps (primary, secondary and facultative tertiary parasitoids of aphids) that naturally colonized the grassland plots. 3. Furthermore, we calculated two ecosystem functions: aphid load (the number of aphid individuals per host plant biomass used as a proxy for herbivory) and parasitism rate. We used structural equation models to explore pathways of direct and indirect effects of plant species richness on higher trophic levels. 4. We found that the densities and richness of species at all trophic levels were influenced by changes in plant species richness. The effects were rarely direct, but instead mediated by the abundance and species richness of aphid host plants and subsequent trophic levels. 5. The herbivore and primary parasitoid levels were most directly affected by changes in plant species richness, with highest insect densities and species richness occurring at intermediate plant species richness. The densities and species richness of secondary parasitoids declined linearly with plant species richness owing to sparser resources, resulting in shorter food chains in communities with the highest plant species richness. 6. Aphid load was highest at intermediate plant species richness and negatively affected by both host plant biomass and host plant species richness. Parasitism rate was mostly affected indirectly via aphid density and overall only weakly negatively related to plant species richness. 7. Our results demonstrate that plant species richness can have strong cascading effects up to high trophic levels. However, their direction may differ at the lower and higher ends of the plant species richness spectrum, cautioning against simplifying consequences of plant species loss for specialist food webs that may become limited by sparse resources at high plant richness.

Indirect interactions in aphid–parasitoid communities

AbstractIndirect interactions between populations of different species can be important in structuring natural communities. Indirect effects are either mediated by changes in population densities (trophic or density‐mediated effects) or by changes in the behavior of species that are not trophically connected (behavioral or trait‐mediated effects). We reviewed the literature on aphids and their parasitoids to explore the various possible indirect interactions that can occur in such communities. The review was motivated by our study of a particular aphid–parasitoid community in a natural (i.e., nonagricultural) habitat, and by the wealth of information that exists about aphid–parasitoid systems in agricultural settings. We focused our review on aphid–parasitoid interactions, but considered how these were influenced by the other aphid natural enemies and also by aphid mutualists and host plants. We conclude that indirect effects are likely to have a major effect in structuring aphid–parasitoid communities, and that the latter are a valuable model system for testing ideas about community interactions.