Jason D. Hoeksema

Linking biodiversity to ecosystem function: implications for conservation ecology

Abstract We evaluate the empirical and theoretical support for the hypothesis that a large proportion of native species richness is required to maximize ecosystem stability and sustain function. This assessment is important for conservation strategies because sustenance of ecosystem functions has been used as an argument for the conservation of species. If ecosystem functions are sustained at relatively low species richness, then arguing for the conservation of ecosystem function, no matter how important in its own right, does not strongly argue for the conservation of species. Additionally, for this to be a strong conservation argument the link between species diversity and ecosystem functions of value to the human community must be clear. We review the empirical literature to quantify the support for two hypotheses: (1) species richness is positively correlated with ecosystem function, and (2) ecosystem functions do not saturate at low species richness relative to the observed or experimental diversity. Few empirical studies demonstrate improved function at high levels of species richness. Second, we analyze recent theoretical models in order to estimate the level of species richness required to maintain ecosystem function. Again we find that, within a single trophic level, most mathematical models predict saturation of ecosystem function at a low proportion of local species richness. We also analyze a theoretical model linking species number to ecosystem stability. This model predicts that species richness beyond the first few species does not typically increase ecosystem stability. One reason that high species richness may not contribute significantly to function or stability is that most communities are characterized by strong dominance such that a few species provide the vast majority of the community biomass. Rapid turnover of species may rescue the concept that diversity leads to maximum function and stability. The role of turnover in ecosystem function and stability has not been investigated. Despite the recent rush to embrace the linkage between biodiversity and ecosystem function, we find little support for the hypothesis that there is a strong dependence of ecosystem function on the full complement of diversity within sites. Given this observation, the conservation community should take a cautious view of endorsing this linkage as a model to promote conservation goals.

A Meta-Analysis of Factors Affecting Local Adaptation between Interacting Species

Adaptive divergence among populations can result in local adaptation, whereby genotypes in native environments exhibit greater fitness than genotypes in novel environments. A body of theory has developed that predicts how different species traits, such as rates of gene flow and generation times, influence local adaptation in coevolutionary species interactions. We used a meta‐analysis of local‐adaptation studies across a broad range of host‐parasite interactions to evaluate predictions about the effect of species traits on local adaptation. We also evaluated how experimental design influences the outcome of local adaptation experiments. In reciprocally designed experiments, the relative gene flow rate of hosts versus parasites was the strongest predictor of local adaptation, with significant parasite local adaptation only in the studies in which parasites had greater gene flow rates than their hosts. When nonreciprocal studies were included in analyses, species traits did not explain significant variation in local adaptation, although the overall level of local adaptation observed was lower in the nonreciprocal than in the reciprocal studies. This formal meta‐analysis across a diversity of host‐parasite systems lends insight into the role of both biology (species traits) and biologists (experimental design) in detecting local adaptation in coevolving species interactions.

Pursuing the big questions about interspecific mutualism: a review of theoretical approaches

Abstract Along with increases in empirical information about interspecific mutualisms have come both new and refined questions about them. These questions have spurred diversification in the theoretical approaches being applied to interspecific mutualism. This theoretical literature has become large and potentially confusing, but as a whole is very relevant to answering the current important questions about mutualism. We first present three important questions about mutualisms raised by recent empirical results. (1) What factors control whether interactions become mutualistic or parasitic? (2) Why are highly specialized mutualisms rare and what are the implications of this observation? (3) What is the impact of trophic complexity on the functioning of mutualisms? Second, we highlight results of recent models of mutualism that address at least one of the three questions, and point to potentially rewarding avenues of exploration for these modeling approaches. This review should be useful to both empiricists and theorists as a roadmap to both the variety of theory currently being applied to mutualisms and to results that are in need of additional theoretical and empirical exploration.

SPECIALIZATION AND RESOURCE TRADE: BIOLOGICAL MARKETS AS A MODEL OF MUTUALISMS

Most ecological theory suggests that the conditions that would give rise to the evolution of mutualisms are rare. In contrast, empirical evidence suggests that mutualisms are common. Thus, there appears to be a need for additional theory to describe conditions under which mutualisms may evolve. Furthermore, there is a need for theory to predict the conditions under which we expect interactions to remain mutualistic once established. We adopt a biological market approach to present a model for the evolution of resource exchange mutualisms, using the relationship between plants and mycorrhizal fungi as an example. We apply the economic theory of relative advantage to investigate the conditions under which species ought to specialize and trade. A simple economic analogy demonstrates that, in a two-resource model, a species that is relatively efficient at acquiring one resource would benefit from specialization on acquisition of that resource accompanied by trade for the other resource. The theory of relative advantage extends this prediction to show that specialization and trade confer an advantage even for species that are relatively poor resource competitors for both resources. Under the assumptions of our model, we show that two species ought to specialize in the acquisition of one resource and trade for a second resource as long as each species perceives different relative acquisition costs for the two resources. We also describe the conditions under which changing resource availabilities will benefit, or harm, both partners in a mutualism. We predict conditions conducive to mutualisms to occur when the costs of resource exchange are low, the opportunity to ensure fair trade is high, or the cost of tolerating cheaters is low. Market models such as ours may help to explain the conditionality often observed in mutualisms.

Ecological persistence of the plant-mycorrhizal mutualism: a hypothesis from species coexistence theory.

In diverse mutualisms, it is common for potential partners to vary in the quality of benefits they provide. When weakly beneficial mutualists and parasites have a competitive advantage over strongly beneficial mutualists, it is not clear how strongly beneficial mutualists persist. If mutualism is destabilized by competitive superiority of weakly beneficial mutualists or cheaters, then mechanisms providing for stable coexistence among competing species may also provide for the persistence of mutualism. We analyze coexistence of species within a mutualist guild using a simple spatial model of patch occupancy to suggest hypotheses about the ecological persistence of mutualism in the interaction between plants and ectomycorrhizal fungi. We suggest that plants could facilitate the persistence of mutualistic mycorrhizal fungi by enhancing the mortality of root tips colonized by competitively superior and less mutualistic fungi. We also discuss previous empirical studies and present original data from field observations in plant‐ectomycorrhizal systems to address our predictions and to suggest profitable avenues for further work.

Expanding comparative-advantage biological market models: contingency of mutualism on partners' resource requirements and acquisition trade-offs.

We expand the comparative–advantage biological market–modelling framework to show how differences between partners, both in their abilities to acquire two resources and in their requirements for those resources, can affect the net benefit of participating in interspecific resource exchange. In addition, the benefits derived from resource trading depend strongly on the nature of the trade–off between the acquisition of one resource and the acquisition of another, described here by the shape (linear, convex or concave) of the resource acquisition constraints of the individuals involved. Combined with previous results, these analyses provide a suite of predictions about whether or not resource exchange is beneficial for two heterospecific individuals relative to a strategy of non–interaction. The benefit derived from resource exchange depends on three factors: (i) relative differences between the partners in their resource acquisition abilities; (ii) relative differences between the partners in their resource requirements; and (iii) variation in the shape of resource acquisition trade–offs. We find that such an explicit consideration of resource requirements and acquisition abilities can provide useful and sometimes non–intuitive predictions about the benefits of resource exchange, and also which resources should be traded by which species.

Ongoing coevolution in mycorrhizal interactions

SUMMARY Coevolution can be a potent force in maintaining and generating biological diversity. Although coevolution is likely to have played a key role in the early development of mycorrhizal interactions, it is unclear how important coevolutionary processes are for ongoing trait evolution in those interactions. Empirical studies have shown that candidate coevolving traits, such as mycorrhizal colonization intensity, exhibit substantial heritable genetic variation within plant and fungal species and are influenced by plant genotype x fungal genotype interactions, suggesting the potential for ongoing coevolutionary selection. Selective source analysis (SSA) could be employed to build on these results, testing explicitly for ongoing coevolutionary selection and analyzing the influence of community context on local coevolutionary selection. Recent empirical studies suggest the potential for coevolution to drive adaptive differentiation among populations of plants and fungi, but further studies, especially using SSA in the context of field reciprocal transplant experiments, are needed to determine the importance of coevolutionary selection compared with nonreciprocal selection on species traits.

From Lilliput to Brobdingnag: Extending Models of Mycorrhizal Function across Scales

ABSTRACT Mycorrhizae occur in nearly all terrestrial ecosystems. Resource exchange between host plants and mycorrhizal fungi influences community, ecosystem, and even global patterns and processes. Understanding the mechanisms and consequences of mycorrhizal symbioses across a hierarchy of scales will help predict system responses to environmental change and facilitate the management of these responses for sustainability and productivity. Conceptual and mathematical models have been developed to help understand and predict mycorrhizal functions. These models are most developed for individual- and population-scale processes, but models at community, ecosystem, and global scales are also beginning to emerge. We review seven types of mycorrhizal models that vary in their scale of resolution and dynamics, and discuss approaches for integrating these models with each other and with general models of terrestrial ecosystems.

Interactions of biotic and abiotic environmental factors in an ectomycorrhizal symbiosis, and the potential for selection mosaics

BackgroundGeographic selection mosaics, in which species exert different evolutionary impacts on each other in different environments, may drive diversification in coevolving species. We studied the potential for geographic selection mosaics in plant-mycorrhizal interactions by testing whether the interaction between bishop pine (Pinus muricata D. Don) and one of its common ectomycorrhizal fungi (Rhizopogon occidentalis Zeller and Dodge) varies in outcome, when different combinations of plant and fungal genotypes are tested under a range of different abiotic and biotic conditions.ResultsWe used a 2 × 2 × 2 × 2 factorial experiment to test the main and interactive effects of plant lineage (two maternal seed families), fungal lineage (two spore collections), soil type (lab mix or field soil), and non-mycorrhizal microbes (with or without) on the performance of plants and fungi. Ecological outcomes, as assessed by plant and fungal performance, varied widely across experimental environments, including interactions between plant or fungal lineages and soil environmental factors.ConclusionThese results show the potential for selection mosaics in plant-mycorrhizal interactions, and indicate that these interactions are likely to coevolve in different ways in different environments, even when initially the genotypes of the interacting species are the same across all environments. Hence, selection mosaics may be equally as effective as genetic differences among populations in driving divergent coevolution among populations of interacting species.

Geographic structure in a widespread plant-mycorrhizal interaction: pines and false truffles

Mutualistic interactions are likely to exhibit a strong geographic mosaic in their coevolutionary dynamics, but the structure of geographic variation in these interactions is much more poorly characterized than in host–parasite interactions. We used a cross‐inoculation experiment to characterize the scales and patterns at which geographic structure has evolved in an interaction between three pine species and one ectomycorrhizal fungus species along the west coast of North America. We found substantial and contrasting patterns of geographic interaction structure for the plants and fungi. The fungi exhibited a clinal pattern of local adaptation to their host plants across the geographic range of three coastal pines. In contrast, plant growth parameters were unaffected by fungal variation, but varied among plant populations and species. Both plant and fungal performance measures varied strongly with latitude. This set of results indicates that in such widespread species interactions, interacting species may evolve asymmetrically in a geographic mosaic because of differing evolutionary responses to clinally varying biotic and abiotic factors.