Cascading effects of early-season herbivory on late-season herbivores and their parasitoids

• Published in: Ecology (Durham) 2016-05, Vol.97 (5), p.1283-1297
• Main Authors: Hernandez-Cumplido, Johnattan, Glauser, Gaetan, Benrey, Betty
• Format: Article
• Language: English
• Subjects: Animals; Apion godmani; Coleoptera - parasitology; Coleoptera - physiology; Defense mechanisms; early‐season herbivory; Food Chain; Herbivores; Herbivory - physiology; host plant‐mediated interactions; Hymenoptera - physiology; induced plant defenses; Insects; Larva - parasitology; Larva - physiology; parasitoid; Phaseolus - physiology; Phaseolus lunatus; Plant ecology; plant fitness; Plant reproduction; Reproduction; Seasons; seed beetle; Seeds; sequential herbivory; Zabrotes subfasciatus
• ISSN: 0012-9658; 1939-9170
• DOI: 10.1890/15-1293.1

There is an increasing awareness that herbivory by one insect species induces changes in a plant that affect the performance of other herbivore species that feed on the same plant. However, previous studies of interspecies interactions mediated by plant defense responses have rarely taken into account different insect guilds or the third trophic level. Using a combination of field and laboratory experiments, we examined how early-season herbivory in lima bean plants (Phaseolus lunatus) by the leaf-chewing herbivore Cerotoma ruficornis and the bean pod weevil Apion godmani affects the abundance and performance of the seed beetle Zabrotes subfasciatus and that of its parasitoid Stenocorse bruchivora, which occurs on the plants at the end of the growing season. In addition, we determined the consequences of early-season herbivore-induced defenses on plant performance. We hypothesized that early-season induction would affect plant reproduction and, hence, would alter the suitability of seeds for late-season seed-eating beetles, and that this would in turn alter the vulnerability of these seed beetles to parasitoids. We found strong support for these hypotheses. In the field, early-season herbivory negatively affected plant reproduction and seeds of these plants suffered lower levels of infestation by seed-eating beetles, which in turn suffered less parasitism. Laboratory assays with field-collected seeds confirmed that the performance of beetles and parasitoids was lower on seeds from plants that had been subjected to early-season herbivory. Further analyses revealed that seeds produced by control plants were larger, heavier, and had a higher concentration of cyanogenic glycosides and total protein content than seeds from plants subjected to herbivory. Our results provide insight into how direct and indirect interactions between and within different trophic levels affect the dynamics and structure of complex communities.