Top-down cascading effects of seed-feeding beetles and their parasitoids on plants and leaf herbivores

When feeding on a plant, herbivorous insects alter the quality of the plant as a food source. This affects other organisms interacting with the same plant. These so-called ‘plant-mediated interactions’ can be altered by parasitoids that attack the herbivores. So far, this research area has mainly focused on interactions at the leaf level, and very little is known about plant-mediated interactions via seeds. It is still poorly understood if seeds that survive insect damage have fewer resources to allocate to plant growth and defence against leaf herbivores, and whether parasitoids that kill seed-feeding insects mitigate such negative effects. Using seeds of wild lima bean plants (Phaseolus lunatus) we studied the effect of the intensity of infestation by seed beetles (Zabrotes subfasciatus) and their parasitoids (Stenocorse bruchivora) on the following parameters under lab conditions: seed mass and germination, plant growth and defensive compounds (cyanogenic glycosides and flavonoids) and performance of a leaf herbivore species (Spodoptera latifascia). In addition, we performed a field experiment using seeds with or without insect damage to investigate the consequences on plant performance and fitness in the wild. Seed beetle infestation had an overall negative impact on seed germination. Lab experiments revealed that damaged seeds produced plants with slower growth and reduced concentration of defensive compounds, which increased the performance of the leaf herbivores. Effects of seed-feeding on seed germination and plant growth were attenuated by parasitism, resulting in a net increase of the number of viable offspring. In the field, we observed that seed damage impaired germination, delayed flowering time and increased leaf herbivory. Our results show that plant-mediated interactions between insect herbivores are not limited to leaf herbivores but extend to seed herbivores. In our study system, parasitoids had no apparent effect on these interactions, despite their strong beneficial effects on germination and plant performance. These findings confirm the long-lasting consequences of indirect plant-mediated interactions in a community-wide ecological context. Furthermore, they contribute to a better understanding of the important but understudied effects of parasitoids on plant fitness.

植食性昆虫取食植物时，会改变植物作为食物资源的品质，进而影响与该植物发生互作的其他生物。这类被称为“植物介导的种间互作”的生态过程，可被攻击植食性昆虫的拟寄生者（parasitoids）所调控。目前该研究领域主要聚焦于叶片层面的种间互作，对于通过种子介导的植物互作却鲜有研究。目前仍存在两个尚未明确的科学问题：其一，遭受昆虫取食后幸存的种子，是否会削减用于植物生长以及抵御叶部植食性昆虫的资源储备；其二，杀死取食种子昆虫的拟寄生者能否缓解此类负面影响。本研究以野生利马豆（Phaseolus lunatus）的种子为实验材料，在实验室条件下探究了四纹豆象（Zabrotes subfasciatus）及其拟寄生者Stenocorse bruchivora的侵染强度对以下参数的影响：种子质量与萌发率、植株生长与防御性化合物（氰苷（cyanogenic glycosides）与黄酮类化合物（flavonoids）），以及叶部植食性昆虫宽条夜蛾（Spodoptera latifascia）的生长表现。此外，本研究还设置了野外控制实验，利用带有或未带有昆虫取食痕迹的种子，探究其对野生状态下植株生长表现与适合度的影响。整体而言，四纹豆象侵染对种子萌发具有显著的负面影响。实验室实验结果显示，源自受损种子的植株生长速率更慢，防御性化合物含量也更低，这一变化提升了叶部植食性昆虫的生长表现。拟寄生作用可缓解取食种子的昆虫对种子萌发与植株生长的负面影响，最终使植株存活后代的数量实现净增长。在野外实验中，我们观察到种子损伤会抑制种子萌发、延迟植株开花时间，并加剧叶部植食性昆虫的取食危害。本研究结果证实，昆虫植食者之间的植物介导互作并不局限于叶部植食性昆虫，而是可延伸至种子植食性昆虫。尽管拟寄生者对种子萌发与植株生长具有显著的有益效应，但在本研究体系中，它们并未对上述种间互作表现出明显的调控作用。这些发现证实了间接植物介导互作在群落尺度生态背景下的长期生态效应。此外，本研究也有助于进一步理解拟寄生者对植物适合度的重要但尚未被充分研究的调控效应。