Floral visitation by the Argentine ant reduces pollinator visitation and seed set in the coast barrel cactus, Ferocactus viridescens

Abstract

Mounting evidence indicates that trade-offs between plant defense and reproduction arise not only from resource allocation but also from interactions among mutualists. Indirect costs of plant defense by ants, for example, can outweigh benefits if ants deter pollinators. Plants can dissuade ants from occupying flowers, but such arrangements may break down when novel ant partners infiltrate mutualisms. Here, we examine how floral visitation by ants affects pollination services when the invasive Argentine ant (Linepithema humile) replaces a native ant species in a food-for-protection mutualism with the coast barrel cactus (Ferocactus viridescens), which, like certain other barrel cacti, produces extrafloral nectar. We compared the effects of floral visitation by the Argentine ant with those of the most prevalent native ant species (Crematogaster californica). Compared to C. californica, the Argentine ant was present in higher numbers in flowers. Cactus bees (Diadasia spp.), the key pollinators in this system, spent less time in flowers when cacti were occupied by the Argentine ant compared to when cacti were occupied by C. californica. Presumably as a consequence of decreased duration of floral visits by Diadasia, cacti occupied by L. humile set fewer seeds per fruit and produced fewer seeds overall compared to cacti occupied by C. californica. These data illustrate the importance of mutualist identity in cases where plants balance multiple mutualisms. Moreover, as habitats become increasingly infiltrated by introduced species, the loss of native mutualists and their replacement by non-native species may alter the shape of trade-offs between plant defense and reproduction.

Balancing anti‐herbivore benefits and anti‐pollinator costs of defensive mutualists

“…Interestingly, dynamic partner transitions allowed plants to maintain relatively high fitness by avoiding the reproductive parasite at reproductive life stages. Previous observational studies have reported negative effects of ant defenders on plant pollination and reproductive success (e.g., Ness 2006, LeVan et al 2013, but the implications of these costs for plant fitness, and hence selection on mutualistic traits, have remained elusive. We provide the first experimental evidence for pollination costs of ant defense and the first assessment of whether and how these costs are balanced by benefits elsewhere in the life cycle.…”

“…Our results add to previous findings that these indicators fail to reveal ecological costs of defensive ''mutualists'' (Ness 2006, Mack and Rudgers 2008, Maleé t al. 2012, LeVan et al 2013) and suggest the need to consider mutualisms in their more realistic, multispecies community context. We report evidence for ecological costs of ant defense, despite the operation of mechanisms that minimize them.…”

“…For example, mutualistic fungal endophytes of plants can reduce colonization of roots by other beneficial microbes (Mack and Rudgers 2008). In food-for-protection mutualisms between ants and plants bearing extrafloral nectar (EFN), the focus of our work, visitation by aggressive ant guards may reduce the frequency of plant-pollinator interactions and, hence, plant reproductive output (Ness 2006, Male´et al 2012, LeVan et al 2013. Thus, ignoring the broader community context may yield incomplete inferences about the fitness consequences of ostensibly beneficial pairwise interactions.…”

“…Evidence for spatial or temporal segregation of ants and open flowers has led to inferences that plants have effectively resolved conflict over pollination (e.g., Stone 1997, Nicklen andWagner 2006). However, few studies have combined deterrence assays with estimates of pollination costs to determine whether mechanisms that isolate ants from floral visitors actually eliminate reproductive costs of ant defense (Willmer and Stone 1997, Ness 2006, LeVan et al 2013.…”

The presence of aggressive ants is associated with fewer insect visits to and altered microbe communities in coffee flowers

“…Aggressive ants also influence the abundance, diversity and composition of other insects that may vector microorganisms. Specifically, aggressive ants (e.g., Argentine ants, red imported fire ants, and pavement ants) are renowned for negatively affecting pollination services in many plant species, both by chasing pollinators (bees) away from plants, stealing nectar without pollinating (Inouye 1980), causing mechanical damage to floral tissue, or leaving deterrent scent marks on flowers (Lach 2007;LeVan, Hung, McCann, Ludka, & Holway 2014;Sidhu & Rankin 2016). In coffee agroecosystems, the dominant arboreal ant Azteca sericeasur tends scale insects on coffee plants, defends scales and coffee plants from both herbivores and predators, and is aggressive towards a number of other ant species .…”