Mismatch managed? Phenological phase extension as a strategy to manage phenological asynchrony in plant–animal mutualisms

Species‐specific shifts in phenology (timing of periodic life cycle events) are occurring with climate change and are already disrupting interactions within and among trophic levels. Phenological phase duration (e.g. beginning to end of flowering) and complementarity (patterns of nonoverlap), and their responses to changing conditions, will be important determinants of species' adaptive capacity to these shifts. Evidence indicates that extension of phenological duration of mutualistic partners could buffer negative impacts that occur with phenological shifts. Therefore, we suggest that techniques to extend the length of phenological duration will contribute to management of systems experiencing phenological asynchrony. Techniques of phenological phase extension discussed include the role of abiotic heterogeneity, genetic and species diversity, and alteration of population timing. We explore these approaches with the goal of creating a framework to build adaptive capacity and address phenological asynchrony in plant–animal mutualisms under climate change.     

Elevated temperatures alter an ant‐aphid mutualism

Ant‐hemipteran mutualisms are keystone interactions that can be variously affected by warming: these mutualisms can be strengthened or weakened, or the species can transition to new mutualist partners. We examined the effects of elevated temperatures on an ant‐aphid mutualism in the subalpine zone of the Rocky Mountains in Colorado, USA. In this system, inflorescences of the host plant, Ligusticum porteri Coult. & Rose (Apiaceae), are colonized by the ant‐tended aphid Aphis asclepiadis Fitch or less frequently by the non‐ant tended aphid Cavariella aegopodii (Scopoli) (both Hemiptera: Aphididae). Using an 8‐year observational study, we tested for two key mechanisms by which ant‐hemipteran mutualisms may be altered by climate change: shifts in species identity and phenological mismatch. Whereas the aphid species colonizing the host plant is not changing in response to year‐to‐year variation in temperature, we found evidence that a phenological mismatch between ants and aphids could occur. In warmer years, colonization of host plant inflorescences by ants is decreased, whereas for A. asclepiadis aphids, host plant colonization is mostly responsive to date of snowmelt. We also experimentally established A. asclepiadis colonies on replicate host plants at ambient and elevated temperatures. Ant abundance did not differ between aphid colonies at ambient vs. elevated temperatures, but ants were less likely to engage in tending behaviors on aphid colonies at elevated temperatures. Sugar composition of aphid honeydew was also altered by experimental warming. Despite reduced tending by ants, aphid colonies at elevated temperatures had fewer intraguild predators. Altogether, our results suggest that higher temperatures may disrupt this ant‐aphid mutualism through both phenological mismatch and by altering benefits exchanged in the interaction.     

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.     

Variable flowering phenology and pollinator use in a community suggest future phenological mismatch

Recent anthropogenic climate change is strongly associated with average shifts toward earlier seasonal timing of activity (phenology) in temperate-zone species. Shifts in phenology have the potential to alter ecological interactions, to the detriment of one or more interacting species. Recent models predict that detrimental phenological mismatch may increasingly occur between plants and their pollinators. One way to test this prediction is to examine data from ecological communities that experience large annual weather fluctuations. Taking this approach, we analyzed interactions over a four-year period among 132 plant species and 665 pollinating insect species within a Mediterranean community. For each plant species we recorded onset and duration of flowering and number of pollinator species. Flowering onset varied among years, and a year of earlier flowering of a species tended to be a year of fewer species pollinating its flowers. This relationship was attributable principally to early-flowering species, suggesting that shifts toward earlier phenology driven by climate change may reduce pollination services due to phenological mismatch. Earlier flowering onset of a species also was associated with prolonged flowering duration, but it is not certain that this will counterbalance any negative effects of lower pollinator species richness on plant reproductive success. Among plants with different life histories, annuals were more severely affected by flowering–pollinator mismatches than perennials. Specialized plant species (those attracting a smaller number of pollinator species) did not experience disproportionate interannual fluctuations in phenology. Thus they do not appear to be faced with disproportionate fluctuations in pollinator species richness, contrary to the expectation that specialists are at greatest risk of losing mutualistic interactions because of climate change.     

Effects of experimental shifts in flowering phenology on plant-pollinator interactions

Climate change has led to phenological shifts in flowering plants and insect pollinators, causing concern that these shifts will disrupt plant-pollinator mutualisms. We experimentally investigated how shifts in flowering onset affect pollinator visitation for 14 native perennial plant species, six of which have exhibited shifts to earlier flowering over the last 70 years and eight of which have not. We manipulated flowering onset in greenhouses and then observed pollinator visitation in the field. Five of six species with historically advanced flowering received more visits when flowering was experimentally advanced, whereas seven of eight species with historically unchanged flowering received fewer visits when flowering earlier. This pattern suggests that species unconstrained by pollinators have advanced their flowering, whereas species constrained by pollinators have not. In contrast to current concern about phenological mismatches disrupting plant-pollinator mutualisms, mismatches at the onset of flowering are not occurring for most of our study species.     

Global warming and the disruption of plant-pollinator interactions

Anthropogenic climate change is widely expected to drive species extinct by hampering individual survival and reproduction, by reducing the amount and accessibility of suitable habitat, or by eliminating other organisms that are essential to the species in question. Less well appreciated is the likelihood that climate change will directly disrupt or eliminate mutually beneficial (mutualistic) ecological interactions between species even before extinctions occur. We explored the potential disruption of a ubiquitous mutualistic interaction of terrestrial habitats, that between plants and their animal pollinators, via climate change. We used a highly resolved empirical network of interactions between 1420 pollinator and 429 plant species to simulate consequences of the phenological shifts that can be expected with a doubling of atmospheric CO₂. Depending on model assumptions, phenological shifts reduced the floral resources available to 17–50% of all pollinator species, causing as much as half of the ancestral activity period of the animals to fall at times when no food plants were available. Reduced overlap between plants and pollinators also decreased diet breadth of the pollinators. The predicted result of these disruptions is the extinction of pollinators, plants and their crucial interactions.     

Ecological theory of mutualism: Robust patterns of stability and thresholds in two‐species population models

Mutualisms are ubiquitous in nature, provide important ecosystem services, and involve many species of interest for conservation. Theoretical progress on the population dynamics of mutualistic interactions, however, comparatively lagged behind that of trophic and competitive interactions, leading to the impression that ecologists still lack a generalized framework to investigate the population dynamics of mutualisms. Yet, over the last 90 years, abundant theoretical work has accumulated, ranging from abstract to detailed. Here, we review and synthesize historical models of two‐species mutualisms. We find that population dynamics of mutualisms are qualitatively robust across derivations, including levels of detail, types of benefit, and inspiring systems. Specifically, mutualisms tend to exhibit stable coexistence at high density and destabilizing thresholds at low density. These dynamics emerge when benefits of mutualism saturate, whether due to intrinsic or extrinsic density dependence in intraspecific processes, interspecific processes, or both. We distinguish between thresholds resulting from Allee effects, low partner density, and high partner density, and their mathematical and conceptual causes. Our synthesis suggests that there exists a robust population dynamic theory of mutualism that can make general predictions.     

Robustness of mutualistic networks under phenological change and habitat destruction

Climate change can alter species phenologies and therefore disrupt species interactions. Habitat destruction can damage biodiversity and population viability. However, we still know very little about the potential effects of these two factors on the diversity and structure of interaction networks when both act simultaneously. Here we developed a mutualistic metacommunity model to explore the effects of habitat destruction and phenological changes on the diversity and structure of plant–pollinator networks. Using an empirical data set of plant and pollinator interactions and their duration in days, we simulated increasing levels of habitat destruction, under projected scenarios of phenological shifts as well for historically recorded changes in phenologies. On one hand, we found that habitat destruction causes catastrophic collapse in global diversity, as well as inducing alternative states. On the other hand, phenological shifts tend to make interactions weaker, increasing local extinction rates. Together, habitat destruction and phenological changes act synergistically, making metacommunities even more vulnerable to global collapse. Metacommunities are also more vulnerable to collapses under scenarios of historical change, in which phenologies are shortened, not just shifted. Furthermore, connectance and nestedness tends to decrease gradually with habitat destruction before the global collapse. Small phenological shifts can raise connectance slightly, due novel interactions appearing in a few generalist species, but larger shifts always reduce connectance. We conclude that the robustness of mutualistic metacommunities against habitat destruction can be greatly impaired by the weakening of positive interactions that results from the loss of phenological overlap.     

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.     

To clean or not to clean: Cleaning mutualism breakdown in a tidal environment

The dynamics and prevalence of mutualistic interactions, which are responsible for the maintenance and structuring of all ecological communities, are vulnerable to changes in abiotic and biotic environmental conditions. Mutualistic outcomes can quickly shift from cooperation to conflict, but it unclear how resilient and stable mutualistic outcomes are to more variable conditions. Tidally controlled coral atoll lagoons that experience extreme diurnal environmental shifts thus provide a model from which to test plasticity in mutualistic behavior of dedicated (formerly obligate) cleaner fish, which acquire all their food resources through client interactions. Here, we investigated cleaning patterns of a model cleaner fish species, the bluestreak wrasse (Labroides dimidiatus), in an isolated tidal lagoon on the Great Barrier Reef. Under tidally restricted conditions, uniquely both adults and juveniles were part‐time facultative cleaners, pecking on Isopora palifera coral. The mutualism was not completely abandoned, with adults also wandering across the reef in search of clients, rather than waiting at fixed site cleaning stations, a behavior not yet observed at any other reef. Contrary to well‐established patterns for this cleaner, juveniles appeared to exploit the system, by biting (“cheating”) their clients more frequently than adults. We show for the first time, that within this variable tidal environment, where mutualistic cleaning might not represent a stable food source, the prevalence and dynamics of this mutualism may be breaking down (through increased cheating and partial abandonment). Environmental variability could thus reduce the pervasiveness of mutualisms within our ecosystems, ultimately reducing the stability of the system.     

On the evolution of non-specific mutualism

It has been argued that mutualisms are non-specific when mutualistic interactions are weak and transient, and become more specific as interactions increase in strength. However, this runs counter to the observation that there exist tightly linked mutualisms of great antiquity that are highly nonspecific. Here we argue that mutualism generates positive, interspecific, frequency-dependent selection, which acts as a cohesive evolutionary force, discouraging evolution of specificity. A simple mathematical model is constructed to analyse the evolution of a community consisting of two guilds of species with mutualistic between-guild interactions, two competing species in each guild and two genetically distinct phenotypes within each species. With some simplifying assumptions, the trajectories in the neighbourhood of the only interior equilibrium point are determined analytically in terms of interactions between individuals. These show that the equilibrium is locally stable (no evolution) when there is little differentiation between phenotypes in mutualistic and interspecific, competitive interactions. On the other hand, when there is strong differentiation between phenotypes in their mutualistic interactions, the equilibrium is unstable and the community starts to evolve towards non-specificity. There are, however, two forces counteracting this tendency which, if sufficiently potent, cause evolution towards specificity. The first is generated by strong differentiation between phenotypes in interspecific competition; the second is caused by specificity which already exists between species in their mutualistic interactions. Thus, the tendency for non-specificity or specificity to evolve depends on the interplay between antagonistic and mutualistic interactions in the community. We illustrate these results with some numerical examples and, finally, survey some data on specificity of mutualisms in the light of the analysis.     

Global stability of obligate mutualism in community modules with facultative mutualists

Mutualism is a fundamental building block of ecological communities and an important driver of biotic evolution. Classic theory suggests that a pairwise two‐species obligate mutualism is fragile, with a large perturbation potentially driving both mutualist populations into extinction. In nature, however, there are many cases of pairwise obligate mutualism. Such pairwise obligate mutualisms are occasionally associated with additional interactions with facultative mutualists. Here, we use a mathematical model to show that when a two‐species obligate mutualism has a single additional link to a third facultative mutualist, the obligate mutualism can become permanently persistent. In the model, a facultative mutualist interacts with one of two inter‐dependent obligate mutualists, and the facultative mutualist enhances the persistence not only of its directly interacting obligate mutualist, but also that of the other obligate mutualist indirectly, enabling the permanent coexistence of the three mutualist species. The effect of the facultative mutualist is strong; it can allow a three‐species permanent coexistence even when two obligate mutualists by themselves are not sustainable (i.e. not locally stable). These results suggest that facultative mutualists can play a pivotal role for the persistence of obligate mutualisms, and contribute to a better understanding on the mechanisms maintaining more complex mutualistic networks of multiple species.     

Phenological responses in a sycamore–aphid–parasitoid system and consequences for aphid population dynamics: A 20 year case study

Species interactions have a spatiotemporal component driven by environmental cues, which if altered by climate change can drive shifts in community dynamics. There is insufficient understanding of the precise time windows during which inter‐annual variation in weather drives phenological shifts and the consequences for mismatches between interacting species and resultant population dynamics—particularly for insects. We use a 20 year study on a tri‐trophic system: sycamore Acer pseudoplatanus, two associated aphid species Drepanosiphum platanoidis and Periphyllus testudinaceus and their hymenopteran parasitoids. Using a sliding window approach, we assess climatic drivers of phenology in all three trophic levels. We quantify the magnitude of resultant trophic mismatches between aphids and their plant hosts and parasitoids, and then model the impacts of these mismatches, direct weather effects and density dependence on local‐scale aphid population dynamics. Warmer temperatures in mid‐March to late‐April were associated with advanced sycamore budburst, parasitoid attack and (marginally) D. platanoidis emergence. The precise time window during which spring weather advances phenology varies considerably across each species. Crucially, warmer temperatures in late winter delayed the emergence of both aphid species. Seasonal variation in warming rates thus generates marked shifts in the relative timing of spring events across trophic levels and mismatches in the phenology of interacting species. Despite this, we found no evidence that aphid population growth rates were adversely impacted by the magnitude of mismatch with their host plants or parasitoids, or direct impacts of temperature and precipitation. Strong density dependence effects occurred in both aphid species and probably buffered populations, through density‐dependent compensation, from adverse impacts of the marked inter‐annual climatic variation that occurred during the study period. These findings explain the resilience of aphid populations to climate change and uncover a key mechanism, warmer winter temperatures delaying insect phenology, by which climate change drives asynchronous shifts between interacting species.     

A conceptual framework for studying the strength of plant–animal mutualistic interactions

The strength of species interactions influences strongly the structure and dynamics of ecological systems. Thus, quantifying such strength is crucial to understand how species interactions shape communities and ecosystems. Although the concepts and measurement of interaction strength in food webs have received much attention, there has been comparatively little progress in the context of mutualism. We propose a conceptual scheme for studying the strength of plant–animal mutualistic interactions. We first review the interaction strength concepts developed for food webs, and explore how these concepts have been applied to mutualistic interactions. We then outline and explain a conceptual framework for defining ecological effects in plant–animal mutualisms. We give recommendations for measuring interaction strength from data collected in field studies based on a proposed approach for the assessment of interaction strength in plant–animal mutualisms. This approach is conceptually integrative and methodologically feasible, as it focuses on two key variables usually measured in field studies: the frequency of interactions and the fitness components influenced by the interactions.     

Kin selection and the Evolution of Mutualisms between Species

Hamilton's theory of kin selection has revolutionized and inspired fifty years of additional theories and experiments on social evolution. Whereas Hamilton's broader intent was to explain the evolutionary stability of cooperation, his focus on shared genetic history appears to have limited the application of his theory to populations within a single species rather than across interacting species. The evolutionary mechanisms for cooperation between species require both spatial and temporal correlations among interacting partners for the benefits to be not only predictable but of sufficient duration to be reliably delivered. As a consequence when the benefits returned by mutualistic partners are redirected to individuals other than the original donor, cooperation usually becomes unstable and parasitism may evolve. However, theoretically, such redirection of mutualistic benefits may actually reinforce, rather than undermine, mutualisms between species when the recipients of these redirected benefits are genetically related to the original donor. Here, I review the few mathematical models that have used Hamilton's theory of kin selection to predict the evolution of mutualisms between species. I go on to examine the applicability of these models to the most well‐studied case of mutualism, pollinating seed predators, where the role of kin selection may have been previously overlooked. Future detailed studies of the direct, and indirect, benefits of mutualism are likely to reveal additional possibilities for applying Hamilton's theory of kin selection to mutualisms between species.     

Biotic interactions and macroevolution: extensions and mismatches across scales and levels

Clade dynamics in the fossil record broadly fit expectations from the operation of competition, predation, and mutualism, but data from both modern and ancient systems suggest mismatches across scales and levels. Indirect effects, as when antagonistic or mutualistic interactions restrict geographic range and thereby elevate extinction risk, are probably widespread and may flow in both directions, as when species- or organismic-level factors increase extinction risk or speciation probabilities. Apparent contradictions across scales and levels have been neglected, including (1) the individualistic geographic shifts of species on centennial and millennial timescales versus evidence for fine-tuned coevolutionary relationships; (2) the extensive and dynamic networks of interactions faced by most species versus the evolution of costly enemy-specific defenses and finely attuned mutualisms; and (3) the macroevolutionary lags often seen between the origin and the diversification of a clade or an evolutionary novelty versus the rapid microevolution of advantageous phenotypes and the invasibility of most communities. Resolution of these and other cross-level tensions presumably hinges on how organismic interactions impinge on genetic population structures, geographic ranges, and the persistence of incipient species, but generalizations are not yet possible. Paleontological and neontological data are both incomplete and so the most powerful response to these problems will require novel integrative approaches. Promising research areas include more realistic approaches to modeling and empirical analysis of large-scale diversity dynamics of ostensibly competing clades; spatial and phylogenetic dissections of clades involved in escalatory dynamics (where prey respond evolutionarily to a broad and shifting array of enemies); analyses of the short- versus long-term consequences of mutualistic symbioses; and fuller use of abundant natural experiments on the evolutionary impacts of ecosystem engineers.     

Warming of experimental plant–pollinator communities advances phenologies,alters traits,reduces interactions and depresses reproduction

Climate change may disrupt plant–pollinator mutualisms by generating phenological asynchronies and by altering traits that shape interaction costs and benefits. Our knowledge is limited to studies that manipulate only one partner or focus on either phenological or trait-based mismatches. We assembled communities of three annual plants and a solitary bee prior to flowering and emergence to test how springtime warming affects phenologies, traits, interactions and reproductive output. Warming advanced community-level flowering onset, peak and end but did not alter bee emergence. Warmed plant communities produced fewer and smaller flowers with less, more-concentrated nectar, reducing attractiveness, and warmed bees were more generalized in their foraging, reducing their effectiveness. Plant–bee interactions were less frequent, shorter and peaked earlier under warming. As a result, warmed plants produced fewer, lighter seeds, indicating pollinator-mediated fitness costs. Climate change will perturb plant–pollinator mutualisms, causing wide-ranging effects on partner species and diminishing the ecosystem service they provide.     

Phytophagous insect-microbe mutualisms and adaptive evolutionary diversification.

Adaptive diversification is a process intrinsically tied to species interactions. Yet, the influence of most types of interspecific interactions on adaptive evolutionary diversification remains poorly understood. In particular, the role of mutualistic interactions in shaping adaptive radiations has been largely unexplored, despite the ubiquity of mutualisms and increasing evidence of their ecological and evolutionary importance. Our aim here is to encourage empirical inquiry into the relationship between mutualism and evolutionary diversification, using herbivorous insects and their microbial mutualists as exemplars. Phytophagous insects have long been used to test theories of evolutionary diversification; moreover, the diversification of a number of phytophagous insect lineages has been linked to mutualisms with microbes. In this perspective, we examine microbial mutualist mediation of ecological opportunity and ecologically based divergent natural selection for their insect hosts. We also explore the conditions and mechanisms by which microbial mutualists may either facilitate or impede adaptive evolutionary diversification. These include effects on the availability of novel host plants or adaptive zones, modifying host-associated fitness trade-offs during host shifts, creating or reducing enemy-free space, and, overall, shaping the evolution of ecological (host plant) specialization. Although the conceptual framework presented here is built on phytophagous insect-microbe mutualisms, many of the processes and predictions are broadly applicable to other mutualisms in which host ecology is altered by mutualistic interactions.     

PHYTOPHAGOUS INSECT–MICROBE MUTUALISMS AND ADAPTIVE EVOLUTIONARY DIVERSIFICATION

Adaptive diversification is a process intrinsically tied to species interactions. Yet, the influence of most types of interspecific interactions on adaptive evolutionary diversification remains poorly understood. In particular, the role of mutualistic interactions in shaping adaptive radiations has been largely unexplored, despite the ubiquity of mutualisms and increasing evidence of their ecological and evolutionary importance. Our aim here is to encourage empirical inquiry into the relationship between mutualism and evolutionary diversification, using herbivorous insects and their microbial mutualists as exemplars. Phytophagous insects have long been used to test theories of evolutionary diversification; moreover, the diversification of a number of phytophagous insect lineages has been linked to mutualisms with microbes. In this perspective, we examine microbial mutualist mediation of ecological opportunity and ecologically based divergent natural selection for their insect hosts. We also explore the conditions and mechanisms by which microbial mutualists may either facilitate or impede adaptive evolutionary diversification. These include effects on the availability of novel host plants or adaptive zones, modifying host-associated fitness trade-offs during host shifts, creating or reducing enemy-free space, and, overall, shaping the evolution of ecological (host plant) specialization. Although the conceptual framework presented here is built on phytophagous insect–microbe mutualisms, many of the processes and predictions are broadly applicable to other mutualisms in which host ecology is altered by mutualistic interactions.     

The evolution of plant-insect mutualisms

Mutualisms (cooperative interactions between species) have had a central role in the generation and maintenance of life on earth. Insects and plants are involved in diverse forms of mutualism. Here we review evolutionary features of three prominent insect-plant mutualisms: pollination, protection and seed dispersal. We focus on addressing five central phenomena: evolutionary origins and maintenance of mutualism; the evolution of mutualistic traits; the evolution of specialization and generalization; coevolutionary processes; and the existence of cheating. Several features uniting very diverse insect-plant mutualisms are identified and their evolutionary implications are discussed: the involvement of one mobile and one sedentary partner; natural selection on plant rewards; the existence of a continuum from specialization to generalization; and the ubiquity of cheating, particularly on the part of insects. Plant-insect mutualisms have apparently both arisen and been lost repeatedly. Many adaptive hypotheses have been proposed to explain these transitions, and it is unlikely that any one of them dominates across interactions differing so widely in natural history. Evolutionary theory has a potentially important, but as yet largely unfilled, role to play in explaining the origins, maintenance, breakdown and evolution of insect-plant mutualisms.