Interaction of pollinators and herbivores on plant fitness suggests a pathway for correlated evolution of mutualism- and antagonism-related traits

Abstract

Different kinds of plant-animal interactions are ordinarily studied in isolation, yet considering the combined fitness effects of mutualistic and antagonistic interactions is essential to understanding plant character evolution. Functional, structural, or phylogenetic associations between attractive and defensive traits may be nonadaptive or result from correlational selection on sets of herbivoryand pollination-linked traits. Nonadditivity of fitness effects of mutualists and antagonists, a requisite for correlational selection, was experimentally tested in the field. We created experimental populations of the insect-pollinated perennial herb, Helleborus foetidus, at 16 different locations distributed among three regions in the Iberian Peninsula. Plants experienced one of four possible selective regimes generated by independently weakening the effects of pollinators and herbivores (flower and fruit predators) according to a two-way fully factorial design. Effects were assessed in terms of number of next-generation offspring recruited per mother plant under natural field conditions. Differences among I nvestigations on the different sorts of plant-animal interactions (e.g., herbivory, pollination, and seed dispersal) have traditionally progressed along separate lanes, the vast majority of studies focusing on just one kind of interaction and ignoring the possible significance of the others. This compartmentalization leads to an artificial oversimplification that may hinder our understanding of the ecology and evolution of plant-animal interactions. It is the composite result of the distinct interactions with all their animal counterparts that plants ''perceive'' in ecological and evolutionary time, and the combined action of different sets of counterparts (e.g., herbivores, pollinators, seed predators, and seed dispersers) exerts intricate ecological and evolutionary influences on plants extending beyond simple additivity of effects (1-5). The combined action of herbivores and pollinators may influence the ecology of plant reproduction and the evolution of pollination-related traits. Through direct or indirect effects on floral displays, flower characteristics, pollen quantity and quality, and plant attractiveness to pollinators, herbivores may ultimately modulate the nature, strength, and fitness consequences of the interaction between plants and their pollinators (6-15). Furthermore, herbivores and pollinators may exert conflicting selective pressures on particular plant traits, and certain characteristics of flowers and inflorescences may reflect compromise adaptations to mutualists and antagonists (5,12,(16)(17)(18)(19)(20).Another possible consequence of the concurrent interaction of plants with herbivores and pollinators that has begun to be recognized recently and the evolutionary origin of which is still poorly understood is the close functional, structural, or phylogenetic association sometimes existing between herbivory-and pollination-related traits. In Hypericum flowers, the same UV pigments play a de...

When ecosystem services interact: crop pollination benefits depend on the level of pest control

“…The seed set benefit obtained from a constant pollination rspb.royalsocietypublishing.org Proc R Soc B 280: 20122243 treatment was larger at high pest control. Similar results have been found in studies with simultaneous manipulations of pollinators and herbivores attacking flowers, fruits or seeds of wild plants [12,28,29]. In these studies, positive interactive effects on plant fitness were attributed to target herbivores cuing in on well-pollinated flowers, or herbivores decreasing plant attractiveness to pollinators.…”

Nectar thieves influence reproductive fitness by altering behaviour of nectar robbers and legitimate pollinators in Corydalis ambigua (Fumariaceae)

“…Interactions among a plant species, its pollinators and its larcenists are embedded in a larger web of interactions. This study provides further evidence that plant-animal interactions in most systems are complex and may include several kinds of interactions occurring simultaneously (Herrera 2000;Bronstein 2001;Ehrl en 2002;Herrera et al 2002;Bronstein, Wilson & Morris 2003). Further, this study has pointed out the fact that nectar larceny could amount to more than a simple ecological curiosity (Berlow 1999;Arizmendi 2001;Newman & Thomson 2005).…”

Attracting Antagonists: Does Floral Nectar Increase Leaf Herbivory?

“…Although plant-herbivore and plant-pollinator interactions have been extensively studied, only recently has it been recognized that the two phenomena are far from independent (e.g., Armbruster 1997, Brody 1997, Strauss 1997, Strauss et al 1999, Adler 2000a, Herrera 2000, Herrera et al 2002. Many plant traits that putatively evolved in the context of herbivore resistance have been shown to influence pollinator preference and/ or visitation.…”