Plant community composition but not plant traits determine the outcome of soil legacy effects on plants and insects

Abstract

Abstract1. Plants leave species-specific legacies in the soil they grow in that can represent changes in abiotic or biotic soil properties. It has been shown that such legacies can affect future plants that grow in the same soil (plant-soil feedback, PSF). Such processes have been studied in detail, but mostly on individual plants. Here, we study PSF effects at the community level and use a trait-based approach both in the conditioning phase and in the feedback phase to study how 12 individual soil legacies influence six plant communities that differ in root size.2. We tested if (1) grassland perennial species with large root systems would leave a stronger legacy than those with small root systems, (2) grass species would leave a more positive soil legacy than forbs, and (3) communities with large root systems would be more responsive than small-rooted communities. We also tested (4) whether a leaf-chewing herbivore and a phloem feeder were affected by soil legacy effects in a community framework.3. Our study shows that the six different plant communities that we used respond differently to soil legacies of 12 different plant species and their functional groups.Species with large root systems did not leave stronger legacies than species with small root systems, nor were communities with large root systems more responsive than communities with root systems.4. Moreover, we show that when communities are affected by soil legacies, these effects carry over to the chewing herbivore Mamestra brassicae (Lepidoptera: Noctuidae) through induced behavioural changes resulting in better performance of a chewing herbivore on forb-conditioned soils than on grass-conditioned soils, whereas performance of the phloem feeder Rhopalosiphum padi (Hemiptera: Aphididae) remained unaffected.5. Synthesis. The results of this study shed light on the variability of soil effects found in previous work on feedbacks in communities. Our study suggests that the composition of plant communities determines to a large part the response to soil legacies.Furthermore, the responses to soil legacies of herbivores feeding on the plant communities that we observed, suggests that in natural ecosystems, the vegetation history may also have an influence on contemporary herbivore assemblages. ThisThis is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Domesticated tomatoes are more vulnerable to negative plant–soil feedbacks than their wild relatives

“…Because the impact of soil associations on plant performance is the net effect of traits that both suppress pathogens and recruit mutualists, either mechanism could be at play. However, the proximate factors mediating plant–soil feedbacks remain unknown; attention has generally focused more on ultimate mechanisms such as plant phylogeny (Fitzpatrick, Gehant, Kotanen, & Johnson, ; Ingerslew & Kaplan, ; Mehrabi & Tuck, ), functional group (Heinen, Sluijs, Biere, Harvey, & Bezemer, ; Ma et al, ) and growth rate (Baxendale, Orwin, Poly, Pommier, & Bardgett, ; Cortois, Schröder‐Georgi, Weigelt, Putten, & Deyn, ). Wild tomatoes possess a diversity of pathogen resistance traits, some, but not all, of which have been introgressed to crop tomatoes via traditional breeding (Bai & Lindhout, ).…”

Effects of Soil Organisms on Aboveground Plant-Insect Interactions in the Field: Patterns, Mechanisms and the Role of Methodology

“…Future studies should also focus on the temporal aspects of above-belowground interactions in the field. As soil communities are dynamic and species-specific soil communities accumulate over time (Diez et al, 2010;Flory and Clay, 2013;Van der Putten et al, 2013;Heinen et al, 2018), it is likely that these temporal dynamics will strongly influence the performance of aboveground insect communities over time. Various controlled studies have shown that the sequence of arrival of aboveground and belowground herbivores on the plant can greatly alter the outcome of soil biota-plant-insect interactions (e.g., Erb et al, 2011;Wang et al, 2014) and to some extent, this has also been shown in field studies (e.g., Gange et al, 2005a), although the link between temporally changing soil communities and temporal variation in aboveground insect communities has not been made.…”

“…Such speciesspecific microbial profiles can influence the performance of other plants that grow later in the same soil (Kostenko et al, 2012;Bezemer et al, 2013;Kos et al, 2015;Heinen et al, 2018). This process is known as plant-soil feedback and can be an important driver of plant community dynamics (Kardol et al, 2006).…”

“…For example, several greenhouse studies have shown that soil legacy effects, the effects of earlier plant growth on the microbial community in the soil, can have strong effects on aboveground herbivores feeding on later growing conspecific plants in those soils (Kostenko et al, 2012;Kos et al, 2015). A recent study, for example, revealed that soil legacies left by grasses and forbs have contrasting effects on a chewing herbivore that fed on plant communities growing on soils with these legacies (Heinen et al, 2018).…”

Conditioning the soil microbiome through plant–soil feedbacks suppresses an aboveground insect pest

“…Plant-soil feedbacks are well studied in the context of succession and invasion ecology to explain how different plant species interact (van der Putten et al, 2013). Notably, several recent studies indicate that plant-soil feedbacks also affect above-ground plant-insect interactions in wild plant species (Kos et al, 2015;Heinen et al, 2018;Hannula et al, 2019). An important question is whether and how plant-soil feedbacks can be used to steer soil microbiomes to increase resistance of later-growing crops to above-ground pests (Kaplan et al, 2018;Mariotte et al, 2018).…”