Conditional Exploitation and Context-Dependent Fitness Consequences of Pollination Mutualisms

Abstract

Mutualisms are classically modeled as obligate, pairwise interactions in which individuals increase each other’s fitness through the exchange of resources or services. Theoretically, the interaction should be unstable because the positive feedback of reciprocal fitness exchange leads to unchecked population growth. Furthermore, the benefit gained by cheating (taking a mutualistic benefit without reciprocating) should be so great that the cheating strategy takes over and the mutualism ceases to persist. Because mutualism is found across the tree of life, identifying the mechanisms permitting mutualism persistence has been a goal for ecologists and evolutionary biologists. In nature, mutualisms are rarely as simplistic as described in the classical models. In particular, they are often complicated by the many direct and indirect interactions within which they are embedded. For example, a species may interact with more than one mutualist simultaneously, and the interaction between those two species will feed back to its own performance. Mutualisms are also prone to exploitation by additional species that render resources or services not provided for them. These individuals directly and indirectly affect the performance of mutualist species. The complexity of the larger network of interactions creates context-dependent outcomes of mutualism: that is, the relative costs and benefits of being a mutualist changes in response to the environment. In order to identify mechanisms of mutualism persistence, it is necessary to understand the context-dependent processes that shape mutualistic interactions. A classic example of mutualism embedded within a larger interaction network is plant-pollinator interactions. Many pollination systems are facultative, and plants and pollinators often interact with more than one species. Floral larcenists, including nectar robbers, exploit floral resources provided to pollinators. The exploitation of floral resources is variable in space and time, making the costs (and relative benefits) to plants and pollinators variable as well. In this study, I examine the context-dependency of pollination mutualisms by quantifying costs and benefits to plants, pollinators, and nectar robbers in different environments. First, I measure the consequences of secondary nectar robbing (foraging for nectar through perforations in floral tissue created by another organism) for male and female reproduction in a hummingbird-pollinated plant, finding significant decreases in female function but not male function. Second, I examine the degree to which primary nectar robbers (organisms that perforate floral tissue) facilitate secondary nectar robbers, given that they are also competing for nectar. I show that the benefit of facilitation does not overcome the cost of competition for secondary nectar-robbing bumble bees, because secondary robbing is in general a more costly behavior than pollinating. Finally, I quantify the cost of inter- and intraspecific competition between a pure pollinator species and a species that acts as a secondary robber in certain contexts. I show that intraspecific competition in each species is stronger than interspecific competition, indicating that the species can coexist. This work advances our knowledge of mutualism by taking into account the net fitness effects for mutualist individuals embedded within a larger interaction network. Understanding these fitness differences allows us to make predictions about resulting population dynamics and make inferences about the stability of mutualism.