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 focussed 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. Read the free Plain Language Summary for this article on the Journal blog.

Automated summary

Herbivorous insects alter the quality of plants as a food source, affecting other organisms interacting with the same plant. This study discovered that seed herbivores can have negative effects on plant growth and defense, but these effects can be mitigated by parasitoids. The study also highlights the positive effects of parasitoids on plant performance and fitness.