Root Herbivores Drive Changes to Plant Primary Chemistry, but Root Loss Is Mitigated under Elevated Atmospheric CO2.

Above- and belowground herbivory represents a major challenge to crop productivity and sustainable agriculture worldwide. How this threat from multiple herbivore pests will change under anthropogenic climate change, via altered trophic interactions and plant response traits, is key to understanding future crop resistance to herbivory. In this study, we hypothesized that atmospheric carbon enrichment would increase the amount (biomass) and quality (C:N ratio) of crop plant resources for above- and belowground herbivore species. In a controlled environment facility, we conducted a microcosm experiment using the large raspberry aphid (Amphorophora idaei), the root feeding larvae of the vine weevil (Otiorhynchus sulcatus), and the raspberry (Rubus idaeus) host-plant. There were four herbivore treatments (control, aphid only, weevil only and a combination of both herbivores) and an ambient (aCO2) or elevated (eCO2) CO2 treatment (390 versus 650 ± 50 µmol/mol) assigned to two raspberry cultivars (cv Glen Ample or Glen Clova) varying in resistance to aphid herbivory. Contrary to our predictions, eCO2 did not increase crop biomass or the C:N ratio of the plant tissues, nor affect herbivore abundance either directly or via the host-plant. Root herbivory reduced belowground crop biomass under aCO2 but not eCO2, suggesting that crops could tolerate attack in a CO2 enriched environment. Root herbivory also increased the C:N ratio in leaf tissue at eCO2, potentially due to decreased N uptake indicated by lower N concentrations found in the roots. Root herbivory greatly increased root C concentrations under both CO2 treatments. Our findings confirm that responses of crop biomass and biochemistry to climate change need examining within the context of herbivory, as biotic interactions appear as important as direct effects of eCO2 on crop productivity.

Global climate change and above- belowground insect herbivore interactions.

Predicted changes to the Earth's climate are likely to affect above-belowground interactions. Our understanding is limited, however, by past focus on two-species aboveground interactions mostly ignoring belowground influences. Despite their importance to ecosystem processes, there remains a dearth of empirical evidence showing how climate change will affect above-belowground interactions. The responses of above- and belowground organisms to climate change are likely to differ given the fundamentally different niches they inhabit. Yet there are few studies that address the biological and ecological reactions of belowground herbivores to environmental conditions in current and future climates. Even fewer studies investigate the consequences of climate change for above-belowground interactions between herbivores and other organisms; those that do provide no evidence of a directed response. This paper highlights the importance of considering the belowground fauna when making predictions on the effects of climate change on plant-mediated interspecific interactions.

Reciprocal feeding facilitation between above- and below-ground herbivores.

Interspecific interactions between insect herbivores predominantly involve asymmetric competition. By contrast, facilitation, whereby herbivory by one insect benefits another via induced plant susceptibility, is uncommon. Positive reciprocal interactions between insect herbivores are even rarer. Here, we reveal a novel case of reciprocal feeding facilitation between above-ground aphids (Amphorophora idaei) and root-feeding vine weevil larvae (Otiorhynchus sulcatus), attacking red raspberry (Rubus idaeus). Using two raspberry cultivars with varying resistance to these herbivores, we further demonstrate that feeding facilitation occurred regardless of host plant resistance. This positive reciprocal interaction operates via an, as yet, unreported mechanism. Specifically, the aphid induces compensatory growth, possibly as a prelude to greater resistance/tolerance, whereas the root herbivore causes the plant to abandon this strategy. Both herbivores may ultimately benefit from this facilitative interaction.

Aboveground-belowground herbivore interactions: a meta-analysis.

Research investigating interactions between aboveground (AG) and below-ground (BG) herbivores has been central to characterizing AG-BG linkages in terrestrial ecosystems, with many of these interactions forming the basis of complex food webs spanning the two subsystems. Despite the growing literature on the effects of AG and BG herbivores on each other, underlying patterns have been difficult to identify due to a high degree of context dependency. In this study, we present the first quantitative meta-analysis of AG and BG herbivore interactions. Previous global predictions, specifically that BG herbivores normally promoted AG herbivore performance and AG herbivores normally reduced BG herbivore performance, were not supported. Instead, the meta-analysis identified four factors that determined the outcome of AG-BG interactions. (1) Sequence of herbivore arrival on host plants was important, with BG herbivores promoting AG herbivore performance only when introduced to the plant simultaneously, whereas AG herbivores had negative effects on BG herbivores only when introduced first. (2) AG herbivores negatively affected BG herbivore survival but tended to increase population growth rates. (3) AG herbivores negatively affected BG herbivore performance on annual plants, but not on perennials, and these effects were observed more consistently in laboratory than field studies. (4) The type of herbivore was also important, with BG insect herbivores belonging to the order Diptera (i.e., true flies) having the strongest negative effects on AG herbivores. Coleoptera (i.e., beetles) species were the most widely investigated BG herbivores and had positive impacts on AG Homoptera (e.g., aphids), but negative effects on AG Hymenoptera (e.g., sawflies). The strongest negative outcomes for BG herbivores were seen when the AG herbivore was a Coleoptera species. We found no evidence for publication bias in AG-BG herbivore interaction literature and conclude that several biological and experimental factors are important for predicting the outcome of AG-BG herbivore interactions. The sequence of herbivore arrival on the host plant was among the most influential.