A mutualism's indirect costs: the most aggressive plant bodyguards also deter pollinators

Abstract

Ness, J. H. 2006. A mutualism's indirect costs: the most aggressive plant bodyguards also deter pollinators. Á Oikos 113: 506 Á514.Plant defenses against herbivores may be costly if they exclude mutualists. Here, I test the hypothesis that aggressive ant bodyguards of plants deter pollinators, and explore mechanisms by which Ferocactus wislizeni , an extrafloral nectary bearing cactus, limits conflicts between its pollinators and bodyguards. Flower visitation by ants and pollinating bees differed among plants tended by four different ant species. The ant species most rarely found in flowers showed the strongest aversion to F. wislizeni flower petals in laboratory assays, suggesting that those structures may include an ant-deterrent. Species-specific estimates of mean ant abundance within flowers and aggressiveness towards other arthropods were used to distinguish the relative threat of ant attack in flowers on plants tended by each ant species. Pollinator surveys in 2003 and 2004 demonstrated that bee visitation rates and the duration of flower occupation differed among plants with different ant associates, decreasing as the threat of ant attack increased. Flowers on plants tended by Solenopsis xyloni , the best ant bodyguard, were more dangerous than those on plants tended by three milder species, due to that ants' greater aggressiveness and abundance within flowers. These flowers were visited by pollinators least frequently and for less time per visit, and produced fruits with significantly lower total seed mass, fewer seeds, and lighter individual seeds, relative to fruits from similarly-sized plants tended by three other ant species. As a result, the best bodyguard may indirectly constrain plant reproduction in some settings. Conflicts between mutualistic guilds may be particularly common in generalized systems, where there is variation in partner quality and in the relative importance of the protection and pollination mutualisms.

The Direct and Ecological Costs of an Ant-Plant Symbiosis

“…However, ants can also impose ecological costs on plants if they negatively affect the interactions between their host plants and other organisms in the environment. For example, ants can deter pollinators (Ness 2006) or increase herbivore loads on their host plants (Frederickson and Gordon 2007;Palmer et al 2008), such as by tending scale insects or aphids (Styrsky and Eubanks 2007). Direct and ecological costs are tightly linked (e.g., investing in ants instead of growth may reduce a plant's competitive ability; see also Heil 2002), but nonetheless we think the distinction is useful because of the different implications of direct and ecological costs for the evolution of cheating.…”

Indirect effects of tending ants on holm oak volatiles and acorn quality

“…5 But, indirect effects have been studied most extensively in the context of trophic cascades when top predators are removed 6 or added 7 and in the context of mutualisms. [8][9][10] Usually, indirect effects are investigated as changes in abundance of the focal species occur. However, indirect effects may result in biologically significant changes in a species that are not reflected only to its abundance.…”

The Ecology of Extrafloral Nectar in Senna mexicana var. chapmanii

“…Flower visits by this insect were significantly more frequent, and their duration significantly longer, on plants with ants present. This result was surprising, as aggressive ants have more often been seen to deter pollinators (Ness 2006;Assunção et al 2014;Ohm and Miller 2014), and pollinators have been observed to recognize the danger posed by ants (Hernández-Cumplido et al 2010;Assunção et al 2014). We are not alone, however, in observing increased pollination rates in the presence of ants.…”

“…These plants, however, receive fewer and shorter visits from pollinators, which are deterred by the same ferocious ants (Ness 2006). Understanding the outcome of ant-plant interactions, therefore, requires that we focus on the broad multi-guild, multi-trophic interactions of which they are a part.…”

“…Indeed, in a few cases ants have even been seen to affect plant defense negatively (Frederickson and Gordon 2007;Mooney 2007;). Conversely, overly aggressive ants may deter beneficial insects such as predators (Torres-Hernandez et al 2000;Nahas et al 2012), parasitoids (Styrsky and Eubanks 2007;), and pollinators (Ness 2006;Hernández-Cumplido et al 2010;Assunção et al 2014). Several studies have shown that pollinators recognize the dangers posed by aggressive ants (Hernández-Cumplido et al 2010, Assunção et al 2014.…”