The exploitation of mutualisms

Mutualisms (interspecific cooperative interactions) are ubiquitously exploited by organisms that obtain the benefits mutualists offer, while delivering no benefits in return. The natural history of these exploiters is well-described, but relatively little effort has yet been devoted to analysing their ecological or evolutionary significance for mutualism. Exploitation is not a unitary phenomenon, but a set of loosely related phenomena: exploiters may follow mixed strategies or pure strategies at either the species or individual level, may or may not be derived from mutualists, and may or may not inflict significant costs on mutualisms. The evolutionary implications of these different forms of exploitation, especially the threats they pose to the stability of mutualism, have as yet been minimally explored. Studies of this issue are usually framed in terms of a "temptation to defect" that generates a destabilizing conflict of interest between partners. I argue that this idea is in fact rather inappropriate for interpreting most observed forms of exploitation in mutualisms. I suggest several alternative and testable ideas for how mutualism can persist in the face of exploitation.     

Three-way coexistence in obligate mutualist-exploiter interactions: the potential role of competition

Many mutualisms host "exploiter" species that consume the benefits provided by one or both mutualists without reciprocating. Exploiters have been widely assumed to destabilize mutualisms, yet they are common. We develop models to explore conditions for local coexistence of obligate plant/pollinating seed parasite mutualisms and nonpollinating exploiters. As the larvae of both pollinators and (at a later time) exploiters consume seeds, we examine the importance of intraspecific and (asymmetric) interspecific competition among and between pollinators and exploiters for achieving three-way coexistence. With weak intra- and interspecific competition, exploiters can invade the stable mutualism and coexist with the mutualists (either stably or with oscillations), provided the exploiters' intrinsic birthrate (b(E)) slightly exceeds that of the pollinators. At higher b(E), all three species go locally extinct. When facing strong interspecific competition, exploiters cannot invade and coexist with the mutualists if intraspecific competition in pollinators and exploiters is weak. However, strong intraspecific competition in pollinators and exploiters facilitates exploiter invasion and coexistence and greatly expands the range of b(E) over which stable coexistence occurs. Our results suggest that mutualist/exploiter coexistence may be more easily achieved than previously thought, thus highlighting the need for a better understanding of competition among and between mutualists and exploiters.     

Evolution and persistence of obligate mutualists and exploiters: competition for partners and evolutionary immunization

Mutualisms are ubiquitous in nature, as is their exploitation by both conspecific and heterospecific cheaters. Yet, evolutionary theory predicts that cheating should be favoured by natural selection. Here, we show theoretically that asymmetrical competition for partners generally determines the evolutionary fate of obligate mutualisms facing exploitation by third-species invaders. When asymmetry in partner competition is relatively weak, mutualists may either exclude exploiters or coexist with them, in which case their co-evolutionary response to exploitation is usually benign. When asymmetry is strong, the mutualists evolve towards evolutionary attractors where they become extremely vulnerable to exploiter invasion. However, exploiter invasion at an early stage of the mutualism's history can deflect mutualists' co-evolutionary trajectories towards slightly different attractors that confer long-term stability against further exploitation. Thus, coexistence of mutualists and exploiters may often involve an historical effect whereby exploiters are co-opted early in mutualism history and provide lasting 'evolutionary immunization' against further invasion.     

Conspicuous extra-floral nectaries are inducible in Vicia faba

Mutualistic interactions are dynamic associations that vary depending on the costs and benefits to each of the interacting parties. Phenotypic plasticity in mutualistic interactions allows organisms to produce rewards to attract mutualists when the benefits of their presence outweigh the costs of producing the rewards. In ant–plant defensive mutualisms, defences are indirect as plants produce extra‐floral nectaries (EFN) to attract predatory ants to deter herbivores. Here we demonstrate that in broad bean, Vicia faba, the overall number of EFNs on a plant increases dramatically following leaf damage. In two damage treatments, removal of: (1) one‐third of one leaf in a single leaf pair or (2) one‐third of both halves of a single leaf pair, resulted in a 59 and 106% increase in the number of EFNs on the plants, respectively, over 1 week. We suggest that the increased production of visually conspicuous EFNs is an adaptive inducible response, to attract predatory arthropods when risk of herbivory increases.     

Host discrimination in modular mutualisms: a theoretical framework for meta-populations of mutualists and exploiters

Plants in multiple symbioses are exploited by symbionts that consume their resources without providing services. Discriminating hosts are thought to stabilize mutualism by preferentially allocating resources into anatomical structures (modules) where services are generated, with examples of modules including the entire inflorescences of figs and the root nodules of legumes. Modules are often colonized by multiple symbiotic partners, such that exploiters that co-occur with mutualists within mixed modules can share rewards generated by their mutualist competitors. We developed a meta-population model to answer how the population dynamics of mutualists and exploiters change when they interact with hosts with different module occupancies (number of colonists per module) and functionally different patterns of allocation into mixed modules. We find that as module occupancy increases, hosts must increase the magnitude of preferentially allocated resources in order to sustain comparable populations of mutualists. Further, we find that mixed colonization can result in the coexistence of mutualist and exploiter partners, but only when preferential allocation follows a saturating function of the number of mutualists in a module. Finally, using published data from the fig–wasp mutualism as an illustrative example, we derive model predictions that approximate the proportion of exploiter, non-pollinating wasps observed in the field.     

Parrots as key multilinkers in ecosystem structure and functioning

Mutually enhancing organisms can become reciprocal determinants of their distribution, abundance, and demography and thus influence ecosystem structure and dynamics. In addition to the prevailing view of parrots (Psittaciformes) as plant antagonists, we assessed whether they can act as plant mutualists in the dry tropical forest of the Bolivian inter‐Andean valleys, an ecosystem particularly poor in vertebrate frugivores other than parrots (nine species). We hypothesised that if interactions between parrots and their food plants evolved as primarily or facultatively mutualistic, selection should have acted to maximize the strength of their interactions by increasing the amount and variety of resources and services involved in particular pairwise and community–wide interaction contexts. Food plants showed different growth habits across a wide phylogenetic spectrum, implying that parrots behave as super‐generalists exploiting resources differing in phenology, type, biomass, and rewards from a high diversity of plants (113 species from 38 families). Through their feeding activities, parrots provided multiple services acting as genetic linkers, seed facilitators for secondary dispersers, and plant protectors, and therefore can be considered key mutualists with a pervasive impact on plant assemblages. The number of complementary and redundant mutualistic functions provided by parrots to each plant species was positively related to the number of different kinds of food extracted from them. These mutually enhancing interactions were reflected in species‐level properties (e.g., biomass or dominance) of both partners, as a likely consequence of the temporal convergence of eco‐(co)evolutionary dynamics shaping the ongoing structure and organization of the ecosystem. A full assessment of the, thus far largely overlooked, parrot–plant mutualisms and other ecological linkages could change the current perception of the role of parrots in the structure, organization, and functioning of ecosystems.     

The mismatch in distributions of vertebrates and the plants that they disperse

Little is known about how mutualistic interactions affect the distribution of species richness on broad geographic scales. Because mutualism positively affects the fitness of all species involved in the interaction, one hypothesis is that the richness of species involved should be positively correlated across their range, especially for obligate relationships. Alternatively, if mutualisms involve multiple mutualistic partners, the distribution of mutualists should not necessarily be related, and patterns in species distributions might be more strongly correlated with environmental factors. In this study, we compared the distributions of plants and vertebrate animals involved in seed‐dispersal mutualisms across the United States and Canada. We compiled geographic distributions of plants dispersed by frugivores and scatter‐hoarding animals, and compared their distribution of richness to the distribution in disperser richness. We found that the distribution of animal dispersers shows a negative relationship to the distribution of the plants that they disperse, and this is true whether the plants dispersed by frugivores or scatter‐hoarders are considered separately or combined. In fact, the mismatch in species richness between plants and the animals that disperse their seeds is dramatic, with plants species richness greatest in the in the eastern United States and the animal species richness greatest in the southwest United States. Environmental factors were corelated with the difference in the distribution of plants and their animal mutualists and likely are more important in the distribution of both plants and animals. This study is the first to describe the broad‐scale distribution of seed‐dispersing vertebrates and compare the distributions to the plants they disperse. With these data, we can now identify locations that warrant further study to understand the factors that influence the distribution of the plants and animals involved in these mutualisms.     

Genetic architecture of multiple mutualisms and mating system in Turnera ulmifolia

Plants often associate with multiple arthropod mutualists. These partners provide important services to their hosts, but multiple interactions can constrain a plant's ability to respond to complex, multivariate selection. Here, we quantified patterns of genetic variance and covariance among rewards for pollination, biotic defence and seed dispersal mutualisms in multiple populations of Turnera ulmifolia to better understand how the genetic architecture of multiple mutualisms might influence their evolution. We phenotyped plants cultivated from 17 Jamaican populations for several mutualism and mating system-related traits. We then fit genetic variance–covariance (G) matrices for the island metapopulation and the five largest individual populations. At the metapopulation level, we observed significant positive genetic correlations among stigma–anther separation, floral nectar production and extrafloral nectar production. These correlations have the potential to significantly constrain or facilitate the evolution of multiple mutualisms in T. ulmifolia and suggest that pollination, seed dispersal and defence mutualisms do not evolve independently. In particular, we found that positive genetic correlations between floral and extrafloral nectar production may help explain their stable coexistence in the face of physiological trade-offs and negative interactions between pollinators and ant bodyguards. Locally, we found only small differences in G among our T. ulmifolia populations, suggesting that geographic variation in G may not shape the evolution of multiple mutualisms.     

Exclusive rewards in mutualisms: ant proteases and plant protease inhibitors create a lock–key system to protect Acacia food bodies from exploitation

Myrmecophytic Acacia species produce food bodies (FBs) to nourish ants of the Pseudomyrmex ferrugineus group, with which they live in an obligate mutualism. We investigated how the FBs are protected from exploiting nonmutualists. Two‐dimensional gel electrophoresis of the FB proteomes and consecutive protein sequencing indicated the presence of several Kunitz‐type protease inhibitors (PIs). PIs extracted from Acacia FBs were biologically active, as they effectively reduced the trypsin‐like and elastase‐like proteolytic activity in the guts of seed‐feeding beetles (Prostephanus truncatus and Zabrotes subfasciatus), which were used as nonadapted herbivores representing potential exploiters. By contrast, the legitimate mutualistic consumers maintained high proteolytic activity dominated by chymotrypsin 1, which was insensitive to the FB PIs. Larvae of an exploiter ant (Pseudomyrmex gracilis) taken from Acacia hosts exhibited lower overall proteolytic activity than the mutualists. The proteases of this exploiter exhibited mainly elastase‐like and to a lower degree chymotrypsin 1‐like activity. We conclude that the mutualist ants possess specifically those proteases that are least sensitive to the PIs in their specific food source, whereas the congeneric exploiter ant appears partly, but not completely, adapted to consume Acacia FBs. By contrast, any consumption of the FBs by nonadapted exploiters would effectively inhibit their digestive capacities. We suggest that the term ‘exclusive rewards’ can be used to describe situations similar to the one that has evolved in myrmecophytic Acacia species, which reward mutualists with FBs but safeguard the reward from exploitation by generalists by making the FBs difficult for the nonadapted consumer to use.     

Does having multiple partners weaken the benefits of facultative mutualism? A test with cacti and cactus‐tending ants

Interspecific facultative mutualisms typically involve guilds of interacting species, and species within a guild can vary in the quality of services they provide. For plants that secrete extrafloral nectar (EFN), visitation by multiple ant species that vary in anti–herbivore abilities may result in reduced benefits, relative to an exclusive association with a high-quality mutualist. This raises the intriguing problem of how facultative ant-plant mutualisms persist, given that EFN is costly to produce, yet may confer diminishing returns as partner diversity increases. I tested the prediction that association with two ant partners ( Crematogaster opuntiae and Liometopum apiculatum ) weakens benefits to the EFN-producing tree cholla cactus ( Opuntia imbricata ). I found that only one ant ( L. apiculatum ) provided protection against herbivores and seed predators. However, this species associated with cacti more frequently than Crematogaster across multiple temporal scales. Within years, Liometopum showed greater constancy on plants they occupied, more frequently colonized vacant plants, and replaced but were never replaced by Crematogaster . Across years of plant development, Liometopum was more abundant on reproductive plants and showed greater overlap with cactus enemies. Simulations of cactus lifetime reproductive output indicated that associating with high- and low-quality mutualists did not significantly reduce plant benefits relative to an exclusive L. apiculatum – O. imbricata association. The results suggest that non-random interaction frequencies, possibly driven by competition, may contribute to the maintenance of facultative mutualisms involving multiple, qualitatively different partners.     

HOW TO PREVENT CHEATING: A DIGESTIVE SPECIALIZATION TIES MUTUALISTIC PLANT-ANTS TO THEIR ANT-PLANT PARTNERS

Mutualisms often involve reciprocal adaptations of both partners. Acacia ant-plants defended by symbiotic Pseudomyrmex ant mutualists secrete sucrose-free extrafloral nectar, which is unattractive to generalists. We aimed to investigate whether this extrafloral nectar can also exclude exploiters, that is nondefending ant species. Mutualist workers discriminated against sucrose whereas exploiters and generalists with no affinity toward Acacia myrmecophytes preferred sucrose, because mutualist workers lacked the sucrose-cleaving enzyme invertase, which is present in workers of the other two groups. Sucrose uptake induced invertase activity in workers of parasites and generalists, but not mutualists, and in larvae of all species: the mutualists loose invertase during their ontogeny. This reduced metabolic capacity ties the mutualists to their plant hosts, but it does not completely prevent the mutualism from exploitation. We therefore investigated whether the exploiters studied here are cheaters (i.e., have evolved from former mutualists) or parasites (exploiters with no mutualistic ancestor). A molecular phylogeny demonstrates that the exploiter species did not evolve from former mutualists, and no evidence for cheaters was found. We conclude that being specialized to their partner can prevent mutualists from becoming cheaters, whereas other mechanisms are required to stabilize a mutualism against the exploitation by parasites.     

Decreasing water availability across the globe improves the effectiveness of protective ant–plant mutualisms: a meta‐analysis

Abiotic conditions can increase the costs of services and/or the benefits of rewards provided by mutualistic partners. Consequently, in some situations, the outcome of mutualisms can move from beneficial to detrimental for at least one partner. In the case of protective mutualisms between ant bodyguards and plants bearing extrafloral nectaries (EFNs), plants from arid environments face a trade‐off between EFN production and maintenance and water and carbon economy. This trade‐off may increase EFN costs and decrease their value as a defensive strategy to plants in such environments. Despite this, the presence of EFNs is an ubiquitous trait in plants from arid environments, suggesting that they provide greater benefits to plants in these environments to compensate for their higher costs. We used a meta‐analysis to investigate if such benefits do increase with decreasing water availability and the possible underlying causes (such as ant behaviour or ant diversity). As predicted, ant effect on EFN plants performance increased as mean annual precipitation decreased. We also found that the frequency of dominant ants on EFN plants increased in drier areas. Due to the more aggressive behaviour of dominant ants, we suggest that they represent an important factor shaping the adaptive value of EFNs to plants in arid environments.     

Invasive belowground mutualists of woody plants

Most plants require mutualistic associations to survive, which can be an important limitation on their ability to become invasive. There are four strategies that permit plants to become invasive without being limited by a lack of mutualists. One is to not be dependent on mutualists. The other three strategies are to form novel mutualisms, form associations with cosmopolitan species, or co-invade with mutualists from their native range. Historically there has been a bias to study mutualisms from a plant perspective, with little consideration of soil biota as invasive species in their own right. Here we address this by reviewing the literature on belowground invasive mutualists of woody plants. We focus on woody invaders as ecosystem-transforming plants that frequently have a high dependence on belowground mutualists. We found that co-invasions are common, with many ectomycorrhizal plant species and N-fixing species co-invading with their mutualists. Other groups, such as arbuscular mycorrhizal plants, tend to associate with cosmopolitan fungal species or to form novel associations in their exotic range. Only limited evidence exists of direct negative effects of co-invading mutualists on native mutualist communities, and effects on native plants appear to be largely driven by altered environmental conditions rather than direct interactions. Mutualists that introduce novel ecosystem functions have effects greater than would be predicted based solely on their biomass. Focusing on the belowground aspects of plant invasions provides novel insights into the impacts, processes and management of invasions of both soil organisms and woody plant species.     

Effects of a belowground mutualism on an aboveground mutualism

Studies of multitrophic interactions between below‐ and aboveground communities have generally focused on soil organisms and antagonists of plant shoots and leaves (herbivores). Despite the widespread occurrence of plant mutualists below‐ and aboveground which can occur on the same host plant, the potential for interactions between them has not been considered. Here we demonstrate that aboveground plant mutualists, insect pollinators, are strongly influenced by belowground plant mutualists, arbuscular mycorrhizal fungi. The presence of arbuscular mycorrhizal fungi in the roots of Chamerion angustifolium increased pollinator visitation and per cent seed set of this plant in the field by up to two times compared with non‐mycorrhizal plants. We propose that interactions between belowground and aboveground mutualisms are widespread and may play important functional roles in populations and communities.     

Mutualism meltdown in insects: bacteria constrain thermal adaptation

Predicting whether and how organisms will successfully cope with climate change presents critical questions for biologists and environmental scientists. Models require knowing how organisms interact with their abiotic environment, as well understanding biotic interactions that include a network of symbioses in which all species are embedded. Bacterial symbionts of insects offer valuable models to examine how microbes can facilitate and constrain adaptation to a changing environment. While some symbionts confer plasticity that accelerates adaptation, long-term bacterial mutualists of insects are characterized by tight lifestyle constraints, genome deterioration, and vulnerability to thermal stress. These essential bacterial partners are eliminated at high temperatures, analogous to the loss of zooanthellae during coral bleaching. Recent field-based studies suggest that thermal sensitivity of bacterial mutualists constrains insect responses. In this sense, highly dependent mutualisms may be the Achilles' heel of thermal responses in insects.     

A general framework for effectiveness concepts in mutualisms

A core interest in studies of mutualistic interactions is the ‘effectiveness’ of mutualists in providing benefits to their partners. In plant‐animal mutualisms it is widely accepted that the total effect of a mutualist on its partner is estimated as (1) a ‘quantity’ component multiplied by (2) a ‘quality’ component, although the meanings of ‘effectiveness,’ ‘quantity,’ and ‘quality’ and which terms are applied to these metrics vary greatly across studies. In addition, a similar quantity × quality = total effect approach has not been applied to other types of mutualisms, although it could be informative. Lastly, when a total effect approach has been applied, it has invariably been from a phytocentric perspective, focussing on the effects of animal mutualists on their plant partner. This lack of a common framework of ‘effectiveness’ of mutualistic interactions limits generalisation and the development of a broader understanding of the ecology and evolution of mutualisms. In this paper, we propose a general framework and demonstrate its utility by applying it to both partners in five different types of mutualisms: pollination, seed dispersal, plant protection, rhizobial, and mycorrhizal mutualisms. We then briefly discuss the flexibility of the framework, potential limitations, and relationship to other approaches.     

Constraints on plant signals and rewards to multiple mutualists?

Many plants invest substantial resources in signaling to and rewarding two kinds of ‘interguild’ mutualists, pollinators and seed dispersers. The signals and rewards are expressed via traits of flowers and fruits. Pollinators and seed dispersers could act in synergistic or antagonistic ways to influence selection on these traits. Here, we address the issue of whether plant species might be constrained in signaling to and rewarding multiple mutualists that provide different types of benefits to plants. Specifically, does investment in one type of mutualist limit investment in another? We examined the correlation between flower size and fruit size for 472 plant species spanning three regional floras. Our analyses made the assumption that structure size is related to plant investment in signals and/or rewards. We expect that a constraint due to interguild mutualisms would be evidenced by a negative correlation between flower and fruit size. Instead, we found significantly positive relationships between flower size and fruit size in all three regional floras. These relationships remained robust after correcting for plant evolutionary history using phylogenetically independent contrasts. These patterns may reflect synergies in selection by pollinators and seed dispersers, genetically-based or resource-based constraints on investment in reproductive tissues, and/or an underlying trade-off in structure size versus number.     

Anthropogenic effects on interaction outcomes: examples from insect-microbial symbioses in forest and savanna ecosystems

The influence of humans on ecosystem dynamics has been, and continues to be, profound. Anthropogenic effects are expected to amplify as human populations continue to increase. Concern over these effects has given rise to a large number of studies focusing on impacts of human activities on individual species or on biotic community structure and composition. Lacking are studies on interactions, particularly mutualisms. Because of the role of mutualisms in ecosystem stability, such studies are critically needed if we are to begin to better understand and predict the responses of ecosystems to anthropogenic change. Most organisms are involved in at least one mutualism, and many in several. Mutualisms facilitate the ability of partners to exploit particular habitats and resources, and play a large role in determining ecological boundaries. When change disrupts, enhances, or introduces new organisms into a mutualism, the outcome and stability of the original partnership(s) is altered as are effects of the symbiosis on the community and ecosystem as a whole. In this paper, using examples from six microbe-insect mutualisms in forest and savanna settings, we showcase how varied and complex the responses of mutualisms can be to an equally varied set of anthropogenic influences. We also show how alterations of mutualisms may ramify throughout affected systems. We stress that researchers must be cognizant that many observed changes in the behaviors, abundances, and distributions of organisms due to human activities are likely to be mediated by mutualists which may alter predictions and actual outcomes in significant ways.     

Benefits and costs of floral visitors to Chilopsis linearis: pollen deposition and stigma closure

In pollination mutualisms, nectar-robbers are usually considered antagonists; visitors that enter flowers (legitimate visitors) are usually considered mutualists. However, nectar-robbers may provide some benefits to plants, whereas legitimate visitors may inflict some costs. The costs and benefits of floral visitors to Chilopsis linearis (desert willow) were compared by number of pollen grains deposited and their effect on stigmas. Because these plants are self-incompatible and pollen-limited, they depend on visitors for services by pollinators to reproduce. On a per-visit basis, only one legitimate visitor, Bombus sonorus (bumblebees) generally benefited plants in terms of pollen deposition. However, no species of visitor was consistently beneficial; every one was at least sometimes ineffective in terms of pollen deposition. Chilopsis had sensitive stigmas that closed immediately upon touch and sometimes reopened later. Whether stigmas remained permanently closed or reopened depended on number of pollen grains deposited and tended also to be affected by source either, outcross or self. Legitimate visitors sometimes cost plants by causing stigma closure without depositing enough pollen to set a fruit. When abundant, a visitor such as Apis mellifera (honeybees) that was only occasionally beneficial on a per-visit basis may have provided a greater benefit to plants as a population than a more effective, but rare visitor. In contrast, nectar-robbers did not benefit plants by depositing pollen grains, but they also did not inflict costs on plants by causing stigmas to close without adequate pollen. There are two general implications of these results. First, individuals of species that appear to be mutualists can vary greatly in the benefits that they give to their partners. Second, apparent mutualists can inflict costs on plants that apparent exploiters (nectar-robbers) do not.     

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 'cheating', 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.