Judith L. Bronstein

OUR CURRENT UNDERSTANDING OF MUTUALISM

It is widely believed that mutualisms, interspecific interactions that benefit both species, have been grossly neglected relative to their true importance in nature. I have reviewed the recent primary literature in order to assess quentitatively the frequency of studies of mutualism, the types of questions they address, and their general scientific approach. All articles appearing from 1986 to 1990 in nine major journals that publish ecological and evolutionary research were examined. It is clear that mutualism research is not in fact rare. Studies of interspecific interactions made up about 22% of theover 4500 articles published during this period; of these, about one-quarter investigated some form of mutualism. Over 90% of them investigated plant-animal interactions, primarily pollination (52%) and seed dispersal (31%), a bias probably related in part to the particular journals examined. The diversity of questions addressed in these articles was surprisingly low. The majority (63%) focused simply on identifying the mutualist of some species of interest. Furthermore, almost all studies were unilateral, that is, they focused on only one of the interacting species, plants being studied much more frequently than their animal partners. Mutualism studies do not appear to have focused on mutualism as a form of interaction in the same way as studies of competition and predation. Rather, researchers have treated mutualism primarily as a life history attribute of one of the two partners. Consequently, although an impressive amount of information has accumulated about these interactions, we are still far from achieving an overall picture that transcends the boundaries of particular taxa or comibinations of taxa. Three other obstacles have prevented data on mutualisms from being brought together: the historical isolation of studies of different kinds of mutualism, a nearly total disconnection between mutualism theories and empirical studies, and the unilateral approach almost always used to study these bilateral interactions. I identify eight research questions whose answers have the potential to reveal broad-based generalizations about the evolution and ecology of mutualism.

Mutualisms in a changing world: an evolutionary perspective

Ecology Letters (2010) 13: 1459-1474 ABSTRACT: There is growing concern that rapid environmental degradation threatens mutualistic interactions. Because mutualisms can bind species to a common fate, mutualism breakdown has the potential to expand and accelerate effects of global change on biodiversity loss and ecosystem disruption. The current focus on the ecological dynamics of mutualism under global change has skirted fundamental evolutionary issues. Here, we develop an evolutionary perspective on mutualism breakdown to complement the ecological perspective, by focusing on three processes: (1) shifts from mutualism to antagonism, (2) switches to novel partners and (3) mutualism abandonment. We then identify the evolutionary factors that may make particular classes of mutualisms especially susceptible or resistant to breakdown and discuss how communities harbouring mutualisms may be affected by these evolutionary responses. We propose a template for evolutionary research on mutualism resilience and identify conservation approaches that may help conserve targeted mutualisms in the face of environmental change.

Cheating and the evolutionary stability of mutualisms

Interspecific mutualisms have been playing a central role in the functioning of all ecosystems since the early history of life. Yet the theory of coevolution of mutualists is virtually nonexistent, by contrast with well–developed coevolutionary theories of competition, predator–prey and host–parasite interactions. This has prevented resolution of a basic puzzle posed by mutualisms: their persistence in spite of apparent evolutionary instability. The selective advantage of‘cheatin’, that is, reaping mutualistic benefits while providing fewer commodities to the partner species, is commonly believed to erode a mutualistic interaction, leading to its dissolution or reciprocal extinction. However, recent empirical findings indicate that stable associations of mutualists and cheaters have existed over long evolutionary periods. Here, we show that asymmetrical competition within species for the commodities offered by mutualistic partners provides a simple and testable ecological mechanism that can account for the long–term persistence of mutualisms. Cheating, in effect, establishes a background against which better mutualists can display any competitive superiority. This can lead to the coexistence and divergence of mutualist and cheater phenotypes, as well as to the coexistence of ecologically similar, but unrelated mutualists and cheaters.

How context dependent are species interactions

The net effects of interspecific species interactions on individuals and populations vary in both sign (-, 0, +) and magnitude (strong to weak). Interaction outcomes are context-dependent when the sign and/or magnitude change as a function of the biotic or abiotic context. While context dependency appears to be common, its distribution in nature is poorly described. Here, we used meta-analysis to quantify variation in species interaction outcomes (competition, mutualism, or predation) for 247 published articles. Contrary to our expectations, variation in the magnitude of effect sizes did not differ among species interactions, and while mutualism was most likely to change sign across contexts (and predation least likely), mutualism did not strongly differ from competition. Both the magnitude and sign of species interactions varied the most along spatial and abiotic gradients, and least as a function of the presence/absence of a third species. However, the degree of context dependency across these context types was not consistent among mutualism, competition and predation studies. Surprisingly, study location and ecosystem type varied in the degree of context dependency, with laboratory studies showing the highest variation in outcomes. We urge that studying context dependency per se, rather than focusing only on mean outcomes, can provide a general method for describing patterns of variation in nature.

Population Dynamics and Mutualism: Functional Responses of Benefits and Costs

We develop an approach for studying population dynamics resulting from mutualism by employing functional responses based on density‐dependent benefits and costs. These functional responses express how the population growth rate of a mutualist is modified by the density of its partner. We present several possible dependencies of gross benefits and costs, and hence net effects, to a mutualist as functions of the density of its partner. Net effects to mutualists are likely a monotonically saturating or unimodal function of the density of their partner. We show that fundamental differences in the growth, limitation, and dynamics of a population can occur when net effects to that population change linearly, unimodally, or in a saturating fashion. We use the mutualism between senita cactus and its pollinating seed‐eating moth as an example to show the influence of different benefit and cost functional responses on population dynamics and stability of mutualisms. We investigated two mechanisms that may alter this mutualisms functional responses: distribution of eggs among flowers and fruit abortion. Differences in how benefits and costs vary with density can alter the stability of this mutualism. In particular, fruit abortion may allow for a stable equilibrium where none could otherwise exist.

The Effects of Invasive Ants on Prospective Ant Mutualists

Ants are recognized for their abilities both to engage in mutualistic interactions with diverse taxa, and to invade and dominate habitats outside their native geographic range. Here, we review the effects of invasive ants on three guilds of mutualists: ant-dispersed plants, ant-tended arthropods, and ant-tended plants. We contrast how those three guilds are affected by invasions, how invasive ants differ from native ants in their interactions with those guilds, and how the seven most invasive ant species differ amongst themselves in those interactions. Ant-dispersed plants typically suffer from interactions with invasive ants, a result we attribute to the small size of those ants relative to native seed-dispersing ants. Effects on the ant-tended arthropods and plants were more frequently positive or non-significant, although it is unclear how often these interactions are reciprocally beneficial. For example, invasive ants frequently attack the natural enemies of these prospective mutualists even in the absence of rewards, and may attack those prospective mutualists. Many studies address whether invasive ants provide some benefit to the partner, but few have asked how invasives rank within a hierarchy of prospective mutualists that includes other ant species. Because ant invasions typically result in the extirpation of native ants, this distinction is highly relevant to predicting and managing the effects of such invasions. Interspecific comparisons suggest that invasive ants are poorer partners of ant-dispersed plants than are most other ants, equally effective partners of ant-tended arthropods, and perhaps better partners of ant-tended plants. Last, we note that the invasive ant taxa differ amongst themselves in how they affect these three mutualist guilds, and in how frequently their interactions with prospective mutualists have been studied. The red imported fire ant, Solenopsis invicta, appears particularly likely to disrupt all three mutualistic interactions, relative to the other six invasive species included in this review.

The Costs of Mutualism1

Abstract Mutualisms are of central importance in biological systems. Despite growing attention in recent years, however, few conceptual themes have yet to be identified that span mutualisms differing in natural history. Here I examine the idea that the ecology and evolution of mutualisms are shaped by diverse costs, not only by the benefits they confer. This concept helps link mutualism to antagonisms such as herbivory, predation, and parasitism, interactions defined largely by the existence of costs. I first briefly review the range of costs associated with mutualisms, then describe how one cost, the consumption of seeds by pollinator offspring, was quantified for one fig/pollinator mutualism. I compare this cost to published values for other fig/pollinator mutualisms and for other kinds of pollinating seed parasite mutualisms, notably the yucca/yucca moth interaction. I then discuss four issues that fundamentally complicate comparative studies of the cost of mutualism: problems of knowing how to measure the magnitude of any one cost accurately; problems associated with using average estimates in the absence of data on sources of variation; complications arising from the complex correlates of costs, such as functional linkages between costs and benefits; and problems that arise from considering the cost of mutualism as a unilateral issue in what is fundamentally a reciprocal interaction. The rich diversity of as-yet unaddressed questions surrounding the costs of mutualism may best be investigated via detailed studies of individual interactions.

Synergy of multiple partners, including freeloaders, increases host fitness in a multispecies mutualism.

Understanding cooperation is a central challenge in biology, because natural selection should favor “free-loaders” that reap benefits without reciprocating. For interspecific cooperation (mutualism), most approaches to this paradox focus on costs and benefits of individual partners and the strategies mutualists use to associate with beneficial partners. However, natural selection acts on lifetime fitness, and most mutualists, particularly longer-lived species interacting with shorter-lived partners (e.g., corals and zooxanthellae, tropical trees and mycorrhizae) interact with multiple partner species throughout ontogeny. Determining how multiple partnerships might interactively affect lifetime fitness is a crucial unexplored link in understanding the evolution and maintenance of cooperation. The tropical tree Acacia drepanolobium associates with four symbiotic ant species whose short-term individual effects range from mutualistic to parasitic. Using a long-term dataset, we show that tree fitness is enhanced by partnering sequentially with sets of different ant symbionts over the ontogeny of a tree. These sets include a “sterilization parasite” that prevents reproduction and another that reduces tree survivorship. Trees associating with partner sets that include these “parasites” enhance lifetime fitness by trading off survivorship and fecundity at different life stages. Our results demonstrate the importance of evaluating mutualism within a community context and suggest that lifespan inequalities among mutualists may help cooperation persist in the face of exploitation.

Ant body size predicts dispersal distance of ant-adapted seeds: Implications of small-ant invasions

The services provided within a community can change as the species composition of that community changes. For example, ant–seed dispersal mutualisms can be disrupted in habitats dominated by invasive ants. We propose that this disruption is related to changes in mean ant body size, given that invasive ants are smaller than most native seed-dispersing ants. We demonstrate that the mean and maximum distances that ants transport seeds adapted for ant dispersal increase with worker body size, and that this relationship is an accelerating power function. This pattern is consistent among three ant subfamilies that include most seed-dispersing ants as well as most invasive ant species, is generalizable across ant species and communities, and is independent of diaspore mass. Using a case study, we demonstrate that both the mean body size of seed-collecting ants and seed dispersal distances are decreased in sites invaded by Solenopsis invicta, the imported red fire ant. Furthermore, we demonstrate that the mean si...

Behavioral consequences of innate preferences and olfactory learning in hawkmoth-flower interactions

Spatiotemporal variability in floral resources can have ecological and evolutionary consequences for both plants and the pollinators on which they depend. Seldom, however, can patterns of flower abundance and visitation in the field be linked with the behavioral mechanisms that allow floral visitors to persist when a preferred resource is scarce. To explore these mechanisms better, we examined factors controlling floral preference in the hawkmoth Manduca sexta in the semiarid grassland of Arizona. Here, hawkmoths forage primarily on flowers of the bat-adapted agave, Agave palmeri, but shift to the moth-adapted flowers of their larval host plant, Datura wrightii, when these become abundant. Both plants emit similar concentrations of floral odor, but scent composition, nectar, and flower reflectance are distinct between the two species, and A. palmeri flowers provide six times as much chemical energy as flowers of D. wrightii. Behavioral experiments with both naïve and experienced moths revealed that hawkmoths learn to feed from agave flowers through olfactory conditioning but readily switch to D. wrightii flowers, for which they are the primary pollinator, based on an innate odor preference. Behavioral flexibility and the olfactory contrast between flowers permit the hawkmoths to persist within a dynamic environment, while at the same time to function as the major pollinator of one plant species.