Cucurbit plant defenses against aboveground or belowground insect herbivores are distinct and shaped by eco-evolutionary factors

Authors: THOMPSON, MORGAN - Texas A&M University; RUSSAVAGE, EMILY - Texas A&M University; GARCES, JEREMY - Texas A&M University; BRADFORD, JACK - Texas A&M University; MERRELL, DANIELLE - Texas A&M University; Suh, Charles; HELMS, ANJEL - Texas A&M University

Submitted to: Basic and Applied Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/2/2025
Publication Date: 4/2/2025
Citation: Thompson, M.N., Russavage, E.M., Garces, J.G., Bradford, J.B., Merrell, D., Suh, C.P.-C., Helms, A.M. 2025. Cucurbit plant defenses against aboveground or belowground insect herbivores are distinct and shaped by eco-evolutionary factors. Basic and Applied Ecology. 86:21-31. https://doi.org/10.1016/j.baae.2025.04.002.
DOI: https://doi.org/10.1016/j.baae.2025.04.002

Interpretive Summary: Plants utilize different defense strategies against aboveground and belowground insect pests. These strategies are largely shaped by ecological and evolutionary factors, such as plant domestication or co-evolutionary history between the plant and insect pest. While considerable research has focused on plant defense against belowground pests, comparatively little is known about plant defense responses against aboveground pests. We conducted a series of laboratory and field studies to examine the defense responses of four domesticated plant species (zucchini squash, pumpkin, cucumber, and watermelon) and two wild species (Texas gourd and Buffalo gourd) against aboveground (squash bug) and below ground (striped cucumber beetle) insect pests. All plant species belong to the gourd family (Cucurbitaceae) but differ in their domestication status and co-existence history with these two insect pests. Across all tested cucurbit species, plants were generally more tolerant of herbivory belowground than aboveground, and wild plant species were more resistant than their domesticated counterparts to herbivory aboveground but not belowground. Additionally, plants with a coexistence history with these two insect pests were less resistant to herbivory aboveground and belowground compared to plants that lacked a coexistence history. Collectively, our findings highlight differences in cucurbit plant defense strategies for aboveground and belowground insect pests, further advancing our understanding of ecological and evolutionary factors that may be exploited by plant breeders to improve insect pest management in cucurbits.

Technical Abstract: Plant defense strategies against insect herbivores are classified broadly as resistance or tolerance. Resistance deters insect growth or feeding, while tolerance mitigates negative effects of herbivory on plant fitness. Plant investment into resistance or tolerance strategies likely falls along a continuum and has been shaped by eco-evolutionary factors, such as plant domestication or coexistence histories with herbivores. Relatively little is known about general defense strategies against aboveground foliar herbivores compared to belowground root herbivores. In the current study, we investigated defense strategies of plant species in the gourd family (Cucurbitaceae) against aboveground squash bug (Anasa tristis) or belowground striped cucumber beetle (Acalymma vittatum) herbivory. We selected six cucurbit plant species that differed in domestication status and coexistence history with herbivores: zucchini squash (Cucurbita pepo subsp. pepo), Texas gourd (Cucurbita pepo subsp. texana), pumpkin (Cucurbita maxima), buffalo gourd (Cucurbita foetidissima), cucumber (Cucumis sativus), and watermelon (Citrullus lanatus). For each plant species and herbivore combination, we conducted separate resistance or tolerance assays. We also carried out a field experiment to examine how longer-term herbivory influences plant reproductive and vegetative growth. We observed variation in resistance among cucurbit plant species against aboveground or belowground herbivory. Across species, plants were generally more tolerant of herbivory belowground than aboveground. We determined that wild plants were more resistant than domesticated counterparts to herbivory aboveground but not belowground. Further, plants with an herbivore coexistence history were less resistant to herbivory aboveground or belowground compared to those without. In the field, zucchini plants were more tolerant of longer-term herbivory either aboveground or belowground than watermelon plants. Taken together, our findings highlight differences in plant defense against aboveground or belowground herbivores, advancing understanding of the eco-evolutionary factors shaping plant defense strategies and providing new insights for agricultural pest management in cucurbits.