Lingering Effects of Herbivory and Plant Defenses on Pollinators

Abstract

In order to survive and reproduce, flowering plants must balance the conflicting selective pressures of herbivore avoidance and pollinator attraction. Links between herbivory and reproduction are often attributed to indirect effects of leaf damage on pollination via reductions in floral allocation, or increases in chemical defenses on herbivore-damaged plants. However, the impacts of herbivory on pollinators have the potential to extend beyond initial floral visits when plant defenses impact pollinator health, foraging behavior, and reproductive success. Here, we examine important but underexplored ways in which herbivory may alter floral phenotype and thus impact pollinators. First, we outline genetic and biochemical mechanisms predicted to underlie floral changes following herbivory, as they impact the floral resources (nectar and pollen) sought by pollinators. Next, we discuss how the consumption of secondary compounds might impact pollinator fitness, including carryover effects on subsequent foraging, mating success, and transgenerational effects on offspring. We consider how pollinator health, life history, and coevolutionary history might result in context-dependent impacts of plant defensive chemistry on pollinator fitness. Finally, we call for studies that measure the impact of herbivore-induced plant defenses on the full spectrum of flower visitors, and contrast case studies on conventional pollinators (for example, generalized bees) versus insects whose larvae are herbivores on the same plants that adults pollinate (such as several butterflies and moths). By linking these consequences of herbivory to fitness effects on both herbivores and pollinators, we will better understand how coevolution between plants, herbivores, and pollinators shapes both defensive and reproductive plant traits.

Floral plasticity: Herbivore‐species‐specific‐induced changes in flower traits with contrasting effects on pollinator visitation

“…Thus, despite the repellence of some pollinators by herbivoreinduced changes in flower traits, plants seem to compensate by attracting other pollinators. In this way, defences can be activated without compromising reproduction (Hoffmeister et al, 2016;Lucas-Barbosa et al, 2013;Rusman et al, 2018), even when defence and flower traits are tightly linked (Jacobsen & Raguso, 2018;Lucas-Barbosa, 2016). Alternatively, herbivore-induced changes in flower traits as by-products of the plant's inducible defensive responses may be maintained because they do not affect reproduction (Gould & Lewontin, 1979).…”

“…Likewise, JA is involved in general developmental processes of flowering (Yuan & Zhang, ) and regulates the expression of various flower traits (Avanci, Luche, Goldman, & Goldman, ; Brioudes et al, ; Muhlemann, Klempien, & Dudareva, ; Radhika, Kost, Boland, & Heil, ). Moreover, flower and defence traits are linked via shared genetic or biochemical pathways, via shared resources (Jacobsen & Raguso, ), or via functional responses, where flower traits are involved in defence as well. Flowering plants use floral volatiles to attract pollinators but also natural enemies of herbivores (Lucas‐Barbosa et al, ; Schiestl et al, ), and although pigments colour the flower, they are also toxic for herbivores (Gronquist et al, ).…”

Ecology of Plastic Flowers

“…Plant defence and reproduction appear to be linked because defensive and reproductive traits are correlated [90,108] and the expression of flower traits changes in response to herbivore attack. Various mechanisms have been proposed to explain these links [17,18]. All traits share resources from the limited nutrient pool of the plant and reallocation of resources to defence can impair reproduction [109].…”

“…Because changes in flower traits mediate interactions with multiple flower-associated community members, we need to adopt a community approach to understand flower trait plasticity [6,7,17,18]. In this review, we discuss 1) the current knowledge on the specificity…”

Plant ontogeny determines strength and associated plant fitness consequences of plant‐mediated interactions between herbivores and flower visitors

“…The effects of herbivores on pollinators may be more extensive through indirect interactions mediated by herbivore‐induced plant responses. Defence and reproductive traits are physiologically linked via multiple mechanisms such as resource trade‐offs, shared phytohormonal signalling pathways, shared genetic and biochemical pathways (Jacobsen & Raguso, ; Lucas‐Barbosa, ; Rusman, Lucas‐Barbosa, et al, ). In addition, individual traits can have both defensive and reproductive functions.…”