Neighborhood effects determine plant-herbivore interactions below ground

1. Plant neighbors can strongly influence the interactions between herbivores and focal plants, for instance by providing food of different quality (consumptive effects) or by changing the behavior and metabolism of the herbivore and the focal plant without being consumed (non-consumptive effects). Determining the species-specific contributions of consumptive and non-consumptive effects is important to understand the ecophysiological mechanisms which underlie neighborhood effects. 2. We quantified the impact of nine different grassland plant species on the interaction between Taraxacum officinale and the root-feeding insect Melolontha melolontha. We investigated the contribution of consumptive and non-consumptive effects to the observed patterns, and evaluated the impact of neighboring plants on the growth and physiology of T. officinale upon M. melolontha attack. 3. Melolontha melolontha growth was strongly affected by the presence of different neighboring species. The three grass species increased larval growth when growing with T. officinale, with Poa pratensis having a synergistic effect in the mixture compared to both monocultures. The forb Centaurea stoebe reduced larval growth when growing with T. officinale or alone. The other five species had no measurable impact on larval performance. Based on these results, P. pratensis and C. stoebe were selected for further experiments. 4. Diet-mixing experiments showed that P. pratensis increased M. melolontha growth when offered together with T. officinale, while C. stoebe suppressed it. When feeding was restricted to artificial diet, larval growth was not changed by the presence of P. pratensis or C. stoebe. However, when feeding was restricted to T. officinale, larval growth was increased by both heterospecific neighbors. Biomass and primary metabolism of T. officinale under attack by M. melolontha was also altered by the presence of C. stoebe and P. pratensis. Together, these results show that consumptive and non-consumptive effects can explain the positive effect of P. pratensis. By contrast, the negative effect of C. stoebe is likely driven exclusively by intoxication. 5. Synthesis. The performed experiments suggest that different combinations of consumptive and non-consumptive effects are likely to contribute to the diversity of neighborhood effects in nature. Furthermore, they show that neighborhood effects are important factors in below ground plant-insect interactions.

1. 植物邻体可强烈调控植食性昆虫与目标植物间的互作关系，例如通过提供不同品质的食物产生消耗效应（consumptive effects），或是在未被取食的前提下改变植食昆虫与目标植物的行为与代谢过程，即非消耗效应（non-consumptive effects）。明确消耗效应与非消耗效应的物种特异性贡献，是解析邻体效应背后生态生理机制的核心前提。
2. 本研究量化了9种不同草地植物对蒲公英（Taraxacum officinale）与根食性昆虫欧洲鳃金龟（Melolontha melolontha）之间互作的影响。我们探究了消耗效应与非消耗效应对观测结果的贡献，并评估了邻体植物在欧洲鳃金龟取食胁迫下对蒲公英生长与生理状态的调控作用。
3. 不同邻体植物的存在会显著影响欧洲鳃金龟的生长表现。当与蒲公英混种时，3种禾本科植物可促进幼虫生长，其中草地早熟禾（Poa pratensis）在混播组合中相较于单播处理表现出协同增效效应。而阔叶草本矢车菊（Centaurea stoebe）在与蒲公英混种或单种时，均会抑制幼虫生长。其余5种植物对幼虫的生长表现无显著影响。基于上述结果，本研究选取草地早熟禾与矢车菊开展后续实验。
4. 混合取食实验显示，当与蒲公英同时作为食物来源时，草地早熟禾可促进欧洲鳃金龟幼虫生长，而矢车菊则会抑制其生长。当幼虫仅能取食人工饲料时，草地早熟禾或矢车菊的存在并未改变幼虫生长速率；但当幼虫仅能取食蒲公英时，异种邻体的存在均会提升幼虫生长量。此外，欧洲鳃金龟取食胁迫下蒲公英的生物量与初级代谢过程，也会因矢车菊与草地早熟禾的存在发生显著改变。综上，上述结果表明，消耗效应与非消耗效应可共同解释草地早熟禾的正向邻体效应；而矢车菊的负向邻体效应则可能仅由毒素介导。
5. 综合讨论。本研究的实验结果表明，消耗效应与非消耗效应的不同组合，或可解释自然界中邻体效应的多样性。此外，研究结果还证实，邻体效应是地下植物-昆虫互作过程中的重要调控因子。