Third and fourth trophic level composition shift in an aphid–parasitoid–hyperparasitoid food web limits aphid control in an intercropping system

Abstract

1. Understanding how resource diversification affects ecological interactions, food web structure and ecosystem functioning is essential in both fundamental and applied ecology. While plant diversification strategies (either in-field or around-field) are often proposed in agricultural landscapes as practices to improve the biological control of herbivores by natural enemies, results remain variable and unsure.2. Here, we studied the effect of an in-field diversification practice (the intercropping of leguminous crops within cereal fields, an increasingly common practice but with inconsistent results on biological control) on cereal aphid control and the structure of a cereal aphid-parasitoid-hyperparasitoid food web for 2 years.3. We report that aphid control was not increased in mixed fields, nor was cereal parasitoid diversity and food web complexity. Nevertheless, the provision of alternative hosts in mixed fields led to a functional community composition shift, favouring generalist parasitoid species over specialist ones. 4. Moreover, we observed a higher hyperparasitism rate in mixed fields, suggesting that secondary parasitoids were favoured by alternative resources, which may have disrupted aphid control by primary parasitoids. Synthesis and applications.This study demonstrates that parasitoid community composition shift and increased top-down control by the fourth trophic level can impact parasitoid efficiency to control herbivores. These results highlight the necessity to study fine-scale mechanisms within food webs to be able to set up efficient methods to support biodiversity and associated ecosystem services in agricultural landscapes.

Composition and Food Web Structure of Aphid-Parasitoid Populations on Plum Orchards in Chile

“…and Pachyneuron sp. [ 76 ] Similar to our results, a recent study found a different hyperparasitoid species composition when more plant resources were added (leguminous plants) intercropped with cereals [ 27 ]. This change in parasitoid composition could be explained although the SV treatment had a patchily distributed, non-persistent and vegetational cover (less plant density), but with a higher species richness, being composed mostly of wild gramineous plants and weeds introduced from other plant families, such as Malvaceae and Asteraceae.…”

“…Indeed, neutral, and even negative, effects of natural enemy diversity on the abundance of pests have been observed [ 25 , 26 ]. Increasing plant diversity may also increase potential negative interactions like intraguild predation or hyperparasitism, resulting in lower pest suppression [ 25 , 26 , 27 , 28 ]. It is necessary to better understand the effects of increasing plant diversity on ecosystem functioning by quantifying the functional role of the interactions within insect communities to evaluate the habitat provisioning role in biological control [ 27 , 29 , 30 , 31 ].…”

“…Likewise, a recent study compared the effect of resource diversification with leguminous intercropping in wheat crops on food web complexity and even when they found no differences in the evaluated metrics (e.g., connectance, generality, etc. ), they highlight the importance to consider each specific system including all trophic interacting levels [ 27 ]. On the other hand, little is known on orchards as aphids–parasitoids–hyperparasitoids have barely been addressed in a food web context.…”

Aphid biological control in arable crops via flower strips: The predominant role of food resources over diversity effects

“…This suggests that a high functional dispersion would ‘dilute’ the relative importance of the plants producing nectar exploited by predators (and having a positive mass effect) among other plants providing unexploited resources. High dispersion probably also favoured the fourth trophic level, which includes hyperparasitoids, thereby disrupting aphid control by primary parasitoids, as shown for crop diversification (Jeavons et al, 2021). Indeed, Campbell et al (2012) previously reported that rates of flower visitation by parasitoids were highest in stands of plants bearing only flowers with short corollas and that these rates were much lower in plant stands bearing flowers with more diverse traits, due to higher levels of competition with bumblebees and hoverflies.…”

Exclusion of third-party arthropods conditions the efficiency of an attract and reward strategy against Dysaphis plantaginea in apple orchards

“…The authors explained these contrasting results by the use of non-species-speci c cues, as kairomones and oral resources, that may have antagonistic effect. Indeed, companion plants and semiochemicals may attract intra-or extraguild predators as well as parasitoids and hyperparasitoids (Jeavons et al 2022), decreasing the e ciency of targeted natural enemies, or even attract other pest species or antagonists such as ants (Hambäck et al, 2021;Heil, 2015). In the same line, alternative food resources may act as a diversion, being preferred over the target pest by natural enemies, therefore decreasing biological control (Brown and Mathews 2007).…”