Mutualism has its limits: consequences of asymmetric interactions between a well-defended plant and its herbivorous pollinator

Abstract

Concern for pollinator health often focuses on social bees and their agricultural importance at the expense of other pollinators and their ecosystem services. When pollinating herbivores use the same plants as nectar sources and larval hosts, ecological conflicts emerge for both parties, as the pollinator's services are mitigated by herbivory and its larvae are harmed by plant defences. We tracked individual-level metrics of pollinator health—growth, survivorship, fecundity—across the life cycle of a pollinating herbivore, the common hawkmoth, Hyles lineata , interacting with a rare plant, Oenothera harringtonii , that is polymorphic for the common floral volatile ( R )-(−)-linalool. Linalool had no impact on floral attraction, but its experimental addition suppressed oviposition on plants lacking linalool. Plants showed robust resistance against herbivory from leaf-disc to whole-plant scales, through poor larval growth and survivorship. Higher larval performance on other Oenothera species indicates that constitutive herbivore resistance by O. harringtonii is not a genus-wide trait. Leaf volatiles differed among populations of O. harringtonii but were not induced by larval herbivory. Similarly, elagitannins and other phenolics varied among plant tissues but were not herbivore-induced. Our findings highlight asymmetric plant–pollinator interactions and the importance of third parties, including alternative larval host plants, in maintaining pollinator health. This article is part of the theme issue ‘Natural processes influencing pollinator health: from chemistry to landscapes’.

Scent releasing silicone septa: A versatile method for bioassays with volatiles

“…Using precise emission of a scent also allows the manipulation of natural scent variability. As an example, Salzmann et al (2007) added uniformly scented septa to orchid inflorescences to mask their intraspecific variability in scent and to test the fitness value of natural fragrance variation, and Balbuena et al (2022) added linalool-emitting septa to polymorphic Oenothera flowers to test the effect of linalool emission on pollinator attraction and oviposition by herbivores. Another study tested the importance of interspecies variability in two species of Silene; Waelti et al (2008) added phenylacetaldehyde emitting from septa to the species that normally lacks this compound, to test its importance on ethological floral isolation between two species.…”

Intrafloral patterns of color and scent in Capparis spinosa L. and the ghosts of its selection past

“…Even though floral blends containing linalool can be innately attractive to M. sexta (Riffell et al, 2009 ), the broader association between linalool (including its specific enantiomers) and nocturnal hawkmoths appears to be more complicated. For example, in behavioral experiments using flower‐naïve M. sexta or H. lineata , this compound was found to be innately neutral as a single odorant (Adam et al, 2021 ; Balbuena et al, 2022 , respectively), whereas it can be learned by M. sexta in conditioning experiments (Gage et al, 2013 ). Finally, the experimental addition of linalool to flowers of Oenothera harringtonii W.L.…”

“…Finally, the experimental addition of linalool to flowers of Oenothera harringtonii W.L. Wagner (Onagraceae) reduces oviposition by H. lineata , which represents a pollinating herbivore for this plant (Balbuena et al, 2022 ). Consequently, the functional role of this compound in C. spinosa should not be taken a priori as a hawkmoth attractant, and additional/alternative explanations, such as pleiotropy, behavioral redundancy or defense against antagonists should be considered.…”

Natural processes influencing pollinator health

“…When pollinators use floral resources but their larval stages feed on the foliage of the same plant, there is an ecological conflict and a challenge for the plant to mediate these interactions. Balbuena et al [43] present one such example in Hyles lineata, a common hawkmoth that feeds on the flowers of Oenothera harringtonii whereas the larvae feed on its leaves. They monitored growth, survival and fecundity as individual-level measures of pollinator health and showed that the plant modifies floral and foliar chemistry to optimize the services of pollinators while protecting against herbivory using a complex of constitutive and induced chemical processes.…”