The Galling Truth: Limited Knowledge of Gall-Associated Volatiles in Multitrophic Interactions

Abstract

Galls are the product of enclosed internal herbivory where the gall maker induces a plant structure within which the herbivores complete their development. For successful sustained herbivory, gall makers must (1) suppress the induction of plant defenses in response to herbivory that is usually mediated through the jasmonic acid pathway and involves volatile organic compound (VOC) production, or (2) have mechanisms to cope with herbivory-induced VOCs, or (3) manipulate production of VOCs to their own advantage. Similarly, plants may have mechanisms (1) to avoid VOC suppression or (2) to attract galler enemies such as parasitoids. While research on VOCs involved in plant–herbivore–parasitoid/predator interactions is extensive, this has largely focussed on the impact of piercing, sucking, and chewing external herbivores or their eggs on VOC emissions. Despite the importance of gallers, owing to their damage to many economically valuable plants, the role of volatiles in gall-associated herbivory has been neglected; exceptions include studies on beneficial gallers and their enemies such as those that occur in brood-site pollination mutualisms. This is possibly the consequence of the difficulties inherent with studying internally occurring herbivory. This review examines the evidence for VOCs in galler attraction to host plants, potential VOC suppression by gallers, increased emission from galls and neighboring tissues, attraction of galler enemies, and the role of galler symbionts in VOC production. It suggests a research focus and ways in which studies on galler-associated VOCs can progress from a philatelic approach involving VOC listing toward a more predictive and evolutionary perspective.

Infestation of the gall midgeDasineura oleaeprovides first evidence of induced plant volatiles in olive leaves

“…Previous studies have only investigated fruit HIPV profile due to B. oleae larvae infestation (Alagna et al ., 2016) and the behavioral responses of its parasitoid Psyttalia concolor to olive drupe HIPVs (Giunti et al ., 2016 a ). Moreover, although gallers usually manage to suppress VOCs (Borges, 2018), D. oleae induces a change of the volatile profiles of attacked plants in the amount of emissions and in the released compounds. A blend of 12 VOCs is distinctive of olive leaves infested by D. oleae : DMNT, β-ocimene, α-copaene, β-copaene, cosmene, germacrene D, ( E )-β-guaiene, ( Z , E )-α-farnesene, ( E , E )-α-farnesene, unknown 1, unknown 3, and heptadecane.…”

Fig trees (Ficus spp.) and their pollinating wasps in Universitas Syiah Kuala Campus, Banda Aceh, Indonesia

“…Female wasps carrying pollen (foundresses) enter through a small, bract-lined tunnel (ostiole) when figs become receptive to pollination (B-phase), usually only last for 2-3 days. The females are attracted to pollen-receptive figs by volatiles released by glands on the ostiolar bracts [17,18]. It is commonly considered that the foundress female wasps die inside the fig, but this is not always the case [19].…”

Interactions Between Figs and Gall-Inducing Fig Wasps: Adaptations, Constraints, and Unanswered Questions

“…Glands on ostiolar bracts release volatiles (Souza et al, 2015;Hu et al, 2020) that attract pollinators to pollen-receptive syconia (Hossaert-McKey et al, 2010;Borges, 2016Borges, , 2018. The ostiole usually shuts after pollinators enter, but loosely arranged bracts sometimes allow the now wingless female pollinators to exit and visit other syconia on the same plant (Hu et al, 2010).…”