Crop domestication relaxes both top-down and bottom-up effects on a specialist herbivore

Authors: WANG, XIN-GENG - UNIVERSITY OF CALIFORNIA; Nadel, Hannah; JOHNSON, MARSHALL - UNIVERSITY OF CALIFORNIA; DAANE, KENT - UNIVERSITY OF CALIFORNIA; Hoelmer, Kim; WALTON, V. - Oregon State University; PICKETT, C. - California Department Of Food And Agriculture; SIME, K. - University Of California

Submitted to: Basic and Applied Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/30/2008
Publication Date: 9/18/2008
Citation: Wang, X., Nadel, H., Johnson, M.W., Daane, K.M., Hoelmer, K.A., Walton, V.W., Pickett, C.H., Sime, K.R. 2008. Crop domestication relaxes both top-down and bottom-up effects on a specialist herbivore. Basic and Applied Ecology. 10:216-227.

Interpretive Summary: Domesticated crops differ significantly from their wild ancestors in many characteristics. Modifications from breeding may increase the susceptibility to herbivores and reduce the efficiency of natural enemies. This study investigates the effects of enlarged fruit resulting from domestication on the interactions between the olive (Olea europaea), the olive fruit fly (Bactrocera oleae), and the fly’s natural enemies. Olive trees have been cultivated for over 6,000 years, and the fly is their primary fruit pest. Wild olives in the fly’s native range are very small with thin pulp. The larval parasitoids associated with the olive fly have short ovipositors that are just capable of probing the pulp of wild olives. Parasitoids that specialize on the olive fly tend to have shorter ovipositors than species that also attack other fly species. Olive varieties grown in California vary in fruit size but even the smallest is substantially larger than wild olives. Larval flies tunnel deeper into the olive pulp with each successive instar, so that young larvae feed closer to the surface and older larvae feed correspondingly deeper in the fruit. Female flies prefer large over small fruit when laying eggs and they deposit more eggs on large fruit. Fly larvae also develop faster and grow larger in large fruit. The olive fly specialist parasitoid Psyttalia lounsburyi more efficiently parasitizes hosts in smaller fruit. The opposite relationship between the performance of the fly and its closely-associated parasitoid on fruit of different sizes suggests that selection for large cultivated olives through domestication may be a factor in the invasiveness of the fly, by reducing the effectiveness of larval parasitoids through creation of “enemy-free space” for the fly in large-fruited commercial olives.

Technical Abstract: Crop domestication can lead to a wide array of differences in plant traits when compared with those of wild progenitors. These modifications often increase the susceptibility of domestic plants to herbivores and at the same time reduce the efficiency of natural enemies, thereby relaxing both bottom-up and top-down effects on the herbivores. This study addresses the effects of fruit enlargement resulting from crop cultivation on the tritrophic interactions involving the olive (Olea europaea), the specialist olive fruit fly (Bactrocera oleae), and its parasitoids. Olive trees have been cultivated for over 6,000 years, and B. oleae is their primary fruit pest. Wild olives in the fly’s native range are small (< 2 mm in pulp thickness). The larval parasitoids associated with B. oleae are all characterized by a short ovipositor (< 3 mm). Specialists on B. oleae tend to have short ovipositors than more generalist species. A large variation in fruit size occurs among four major olive cultivars grown in California: ‘Mission’, ‘Manzanilla’, ‘Ascolana’, and ‘Sevillano’. Even the smallest ‘Mission’ is substantially larger than wild olives. Larval B. oleae move deeper into the olive pulp with each successive instar, and the final instar usually tunnels around the seed. There is a positive linear relationship between larval feeding depth and fruit pulp thickness for the old first, second, and third (final) instars. Female flies prefer large to small fruit, laying more eggs and spending more time foraging on large than small fruit in choice tests. Larval flies develop faster and grow larger in large fruit than in small fruit. In contrast, the specialist parasitoid Psyttalia lounsburyi is more efficient in parasitizing hosts in smaller fruit. The inverse relationship between the performance of the fly and its co-evolved parasitoids on fruit of different sizes indicates that enlargement of cultivated olives through domestication may not only favor the invasiveness of the fly, but also limits the accessibility of larval parasitoids and creates an enemy-free space for the fly in large fruit in commercial olives. This may partly explain why the considerable efforts to manage B. oleae using introduced parasitoids (i.e., classical biological control) have not been successful in the Mediterranean basin.