Drought stress influences foraging preference of a solitary bee on two wildflowers.

BACKGROUND AND AIMS: Pollinators provide critical ecosystem services, maintaining biodiversity and benefiting global food production. However, plants, pollinators, and their mutualistic interactions may be affected by drought, which has increased in severity and frequency under climate change. Using two annual, insect-pollinated wildflowers (Phacelia campanularia and Nemophila menziesii), we asked how drought impacts floral traits and foraging preferences of a solitary bee (Osmia lignaria) and explore potential implications for plant reproduction. METHODS: In greenhouses, we experimentally subjected plants to drought to induce water stress, as verified by leaf water potential. To assess the impact of drought on floral traits, we measured flower size, floral display size, nectar volume, and nectar sugar concentration. To explore how drought-induced effects on floral traits affected bee foraging preferences, we performed choice trials. Individual female bees were placed into foraging arenas with two conspecific plants, one droughted and one non-droughted, and were allowed to forage freely. KEY RESULTS: We determined that P. campanularia is more drought-tolerant than N. menziesii based on measures of turgor loss point, and confirmed that droughted plants were more drought-stressed than non-droughted plants. For droughted plants of both species, floral display size was reduced, and flowers were smaller and produced less, more-concentrated nectar. We found that bees preferred non-droughted flowers of N. menziesii. However, bee preference for non-droughted P. campanularia flowers depended on the time of day and was detected only in the afternoon. CONCLUSIONS: Our findings indicate that bees prefer visiting non-droughted flowers, likely reducing pollination success for drought-stressed plants. Lack of preference for non-droughted P. campanularia flowers in the morning may reflect the higher drought tolerance of this species. This work highlights the potentially intersecting, short-term physiological and pollinator behavioral responses to drought and suggests that such responses may reshape plant-pollinator interactions, ultimately reducing reproductive output for less drought-tolerant wildflowers.

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.

Confounding effects of spatial variation on shifts in phenology.

Shifts in the timing of life history events have become an important source of information about how organisms are responding to climate change. Phenological data have generally been treated as purely temporal, with scant attention to the inherent spatial aspects of such data. However, phenological data are tied to a specific location, and considerations of sampling design, both over space and through time, can critically affect the patterns that emerge. Focusing on flowering phenology, we describe how purely spatial shifts, such as adding new study plots, or the colonization of a study plot by a new species, can masquerade as temporal shifts. Such shifts can look like responses to climate change but are not. Furthermore, the same aggregate phenological curves can be composed of individuals with either very different or very similar phenologies. We conclude with a set of recommendations to avoid ambiguities arising from the spatiotemporal duality of phenological data.

Phylogenetic trait-based analyses of ecological networks.

Ecological networks of two interacting guilds of species, such as flowering plants and pollinators, are common in nature, and studying their structure can yield insights into their resilience to environmental disturbances. Here we develop analytical methods for exploring the strengths of interactions within bipartite networks consisting of two guilds of phylogenetically related species. We then apply these methods to investigate the resilience of a plant-pollinator community to anticipated climate change. The methods allow the statistical assessment of, for example, whether closely related pollinators are more likely to visit plants with similar relative frequencies, and whether closely related pollinators tend to visit closely related plants. The methods can also incorporate trait information, allowing us to identify which plant traits are likely responsible for attracting different pollinators. These questions are important for our study of 14 prairie plants and their 22 insect pollinators. Over the last 70 years, six of the plants have advanced their flowering, while eight have not. When we experimentally forced earlier flowering times, five of the six advanced-flowering species experienced higher pollinator visitation rates, whereas only one of the eight other species had more visits; this network thus appears resilient to climate change, because those species with advanced flowering have ample pollinators earlier in the season. Using the methods developed here, we show that advanced-flowering plants did not have a distinct pollinator community from the other eight species. Furthermore, pollinator phylogeny did not explain pollinator community composition; closely related pollinators were not more likely to visit the same plant species. However, differences among pollinator communities visiting different plants were explained by plant height, floral color, and symmetry. As a result, closely related plants attracted similar numbers of pollinators. By parsing out characteristics that explain why plants share pollinators, we can identify plant species that likely share a common fate in a changing climate.

Pollinator effectiveness varies with experimental shifts in flowering time.

The earlier flowering times exhibited by many plant species are a conspicuous sign of climate change. Altered phenologies have caused concern that species could suffer population declines if they flower at times when effective pollinators are unavailable. For two perennial wildflowers, Tradescantia ohiensis and Asclepias incarnata, we used an experimental approach to explore how changing phenology affects the taxonomic composition of the pollinator assemblage and the effectiveness of individual pollinator taxa. After finding in the previous year that fruit set varied with flowering time, we manipulated flowering onset in greenhouses, placed plants in the field over the span of five weeks, and measured pollinator effectiveness as the number of seeds produced after a single visit to a flower. The average effectiveness of pollinators and the expected rates of pollination success were lower for plants of both species flowering earlier than for plants flowering at historical times, suggesting there could be reproductive costs to earlier flowering. Whereas for A. incarnata, differences in average seed set among weeks were due primarily to changes in the composition of the pollinator assemblage, the differences for T. ohiensis were driven by the combined effects of compositional changes and increases over time in the effectiveness of some pollinator taxa. Both species face the possibility of temporal mismatch between the availability of the most effective pollinators and the onset of flowering, and changes in the effectiveness of individual pollinator taxa through time may add an unexpected element to the reproductive consequences of such mismatches.

Legume germination is delayed in dry soils and in sterile soils devoid of microbial mutualists: Species-specific implications for upward range expansions.

Climate change is affecting species and their mutualists and can lead to the weakening or loss of important interspecific interactions. Through independent shifts in partner phenology and distribution, climatic stress can separate mutualists temporally or spatially, leading to alterations in partner functional traits and fitness. Here, we explored the effects of the loss of microbial mutualists on legume germination success and phenology. In particular, we assessed the effects of mutualism loss via soil sterilization, increased drought, and introduction to novel soils found beyond the current distributions of two focal legume species in subalpine environments. Through common garden experiments in controlled environments, we found evidence that soil sterilization (and consequent microbial absence) and dry soils caused species-specific phenological delays of 2-5 weeks in germination, likely as a result of interaction loss between legumes and specialized germination-promoting soil microbes, such as mutualistic rhizobia. Delays in germination caused by a mismatch between legumes and beneficial microbes could negatively affect legume fitness through increased plant-plant competition later in the season. Additionally, we found evidence of the presence of beneficial microbes beyond the current elevational range of one of our focal legumes, which may allow for expansion of the leading edge, although harsh abiotic factors in the alpine may hinder this. Alterations in the strength of soil microbe-legume mutualisms may lead to reduced fitness and altered demography for both soil microbes and legumes.

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.

Changing Climate Drives Divergent and Nonlinear Shifts in Flowering Phenology across Elevations.

Climate change is known to affect regional weather patterns and phenology; however, we lack understanding of how climate drives phenological change across local spatial gradients. This spatial variation is critical for determining whether subpopulations and metacommunities are changing in unison or diverging in phenology. Divergent responses could reduce synchrony both within species (disrupting gene flow among subpopulations) and among species (disrupting interspecific interactions in communities). We also lack understanding of phenological change in environments where life history events are frequently aseasonal, such as the tropical, arid, and semi-arid ecosystems that cover vast areas. Using a 33-year-long dataset spanning a 1,267-m semi-arid elevational gradient in the southwestern United States, we test whether flowering phenology diverged among subpopulations within species and among five communities comprising 590 species. Applying circular statistics to test for changes in year-round flowering, we show flowering has become earlier for all communities except at the highest elevations. However, flowering times shifted at different rates across elevations likely because of elevation-specific changes in temperature and precipitation, indicating diverging phenologies of neighboring communities. Subpopulations of individual species also diverged at mid-elevation but converged in phenology at high elevation. These changes in flowering phenology among communities and subpopulations are undetectable when data are pooled across the gradient. Furthermore, we show that nonlinear changes in flowering times over the 33-year record are obscured by traditional calculations of long-term trends. These findings reveal greater spatiotemporal complexity in phenological responses than previously recognized and indicate climate is driving phenological reshuffling across local spatial gradients.

Parasitism modifies the direct effects of warming on a hemiparasite and its host.

Climate change is affecting interactions among species, including host-parasite interactions. The effects of warming are of particular interest for interactions in which parasite and host physiology are intertwined, such as those between parasitic plants and their hosts. However, little is known about how warming will affect plant parasitic interactions, hindering our ability to predict how host and parasite species will respond to climate change. Here, we test how warming affects aboveground and belowground biomass of a hemiparasitic species (Castilleja sulphurea) and its host (Bouteloua gracilis), asking whether the effects of warming depend on the interaction between these species. We also measured how warming affected the number of haustorial connections between parasite and host. We grew each species alone and together under ambient and warmed conditions. Hosts produced more belowground biomass under warming. However, host biomass was reduced when plants were grown with a hemiparasite. Thus, parasitism negated the benefit of warming on belowground growth of the host. Host resource allocation to roots versus shoots also changed in response to both interaction with the parasite and warming, with hosts producing more root biomass relative to shoot biomass when grown with a parasite and when warmed. As expected, hemiparasite biomass was greater when grown with a host. Warmed parasites had lower root:shoot ratios but only when grown with a host. Under elevated temperatures, hemiparasite aboveground biomass was marginally greater, and plants produced significantly more haustoria. These findings indicate that warming can influence biomass production, both by modifying the interaction between host plants and hemiparasites and by affecting the growth of each species directly. To predict how species will be affected, it is important to understand not only the direct effects of warming but also the indirect effects that are mediated by species interactions. Ultimately, understanding how climate change will affect species interactions is key to understanding how it will affect individual species.

Effects of global change on insect pollinators: multiple drivers lead to novel communities.

Global change drivers, in particular climate change, exotic species introduction, and habitat alteration, affect insect pollinators in numerous ways. In response, insect pollinators show shifts in range and phenology, interactions with plants and other taxa are altered, and in some cases pollination services have diminished. Recent studies show some pollinators are tracking climate change by moving latitudinally and elevationally, while others are not. Shifts in insect pollinator phenology generally keep pace with advances in flowering, although there are exceptions. Recent data demonstrate competition between exotic and native bees, along with rapid positive effects of exotic plant removal on pollinator richness. Genetic analyses tie bee fitness to habitat quality. Across drivers, novel communities are a common outcome that deserves more study.

Plant-pollinator interactions under climate change: The use of spatial and temporal transplants.

Climate change is affecting both the timing of life history events and the spatial distributions of many species, including plants and pollinators. Shifts in phenology and range affect not only individual plant and pollinator species but also interactions among them, with possible negative consequences for both parties due to unfavorable abiotic conditions or mismatches caused by differences in shift magnitude or direction. Ultimately, population extinctions and reductions in pollination services could occur as a result of these climate change-induced shifts, or plants and pollinators could be buffered by plastic or genetic responses or novel interactions. Either scenario will likely involve altered selection pressures, making an understanding of plasticity and local adaptation in space and time especially important. In this review, we discuss two methods for studying plant-pollinator interactions under climate change: spatial and temporal transplants, both of which offer insight into whether plants and pollinators will be able to adapt to novel conditions. We discuss the advantages and limitations of each method and the future possibilities for this area of study. We advocate for consideration of how joint shifts in both dimensions might affect plant-pollinator interactions and point to key insights that can be gained with experimental transplants.

Phenological shifts and the fate of mutualisms.

Climate change is altering the timing of life history events in a wide array of species, many of which are involved in mutualistic interactions. Because many mutualisms can form only if partner species are able to locate each other in time, differential phenological shifts are likely to influence their strength, duration and outcome. At the extreme, climate change-driven shifts in phenology may result in phenological mismatch: the partial or complete loss of temporal overlap of mutualistic species. We have a growing understanding of how, when, and why phenological change can alter one type of mutualism-pollination. However, as we show here, there has been a surprising lack of attention to other types of mutualism. We generate a set of predictions about the characteristics that may predispose mutualisms in general to phenological mismatches. We focus not on the consequences of such mismatches but rather on the likelihood that mismatches will develop. We explore the influence of three key characteristics of mutualism: 1) intimacy, 2) seasonality and duration, and 3) obligacy and specificity. We predict that the following characteristics of mutualism may increase the likelihood of phenological mismatch: 1) a non-symbiotic life history in which co-dispersal is absent; 2) brief, seasonal interactions; and 3) facultative, generalized interactions. We then review the limited available data in light of our a priori predictions and point to mutualisms that are more and less likely to be at risk of becoming phenologically mismatched, emphasizing the need for research on mutualisms other than plant-pollinator interactions. Future studies should explicitly focus on mutualism characteristics to determine whether and how changing phenologies will affect mutualistic interactions.

Physiological effects of climate warming on flowering plants and insect pollinators and potential consequences for their interactions.

Growing concern about the influence of climate change on flowering plants, pollinators, and the mutualistic interactions between them has led to a recent surge in research. Much of this research has addressed the consequences of warming for phenological and distributional shifts. In contrast, relatively little is known about the physiological responses of plants and insect pollinators to climate warming and, in particular, how these responses might affect plant-pollinator interactions. Here, we summarize the direct physiological effects of temperature on flowering plants and pollinating insects to highlight ways in which plant and pollinator responses could affect floral resources for pollinators, and pollination success for plants, respectively. We also consider the overall effects of these responses on plant-pollinator interaction networks. Plant responses to warming, which include altered flower, nectar, and pollen production, could modify floral resource availability and reproductive output of pollinating insects. Similarly, pollinator responses, such as altered foraging activity, body size, and life span, could affect patterns of pollen flow and pollination success of flowering plants. As a result, network structure could be altered as interactions are gained and lost, weakened and strengthened, even without the gain or loss of species or temporal overlap. Future research that addresses not only how plant and pollinator physiology are affected by warming but also how responses scale up to affect interactions and networks should allow us to better understand and predict the effects of climate change on this important ecosystem service.

Phenological overlap of interacting species in a changing climate: an assessment of available approaches.

Concern regarding the biological effects of climate change has led to a recent surge in research to understand the consequences of phenological change for species interactions. This rapidly expanding research program is centered on three lines of inquiry: (1) how the phenological overlap of interacting species is changing, (2) why the phenological overlap of interacting species is changing, and (3) how the phenological overlap of interacting species will change under future climate scenarios. We synthesize the widely disparate approaches currently being used to investigate these questions: (1) interpretation of long-term phenological data, (2) field observations, (3) experimental manipulations, (4) simulations and nonmechanistic models, and (5) mechanistic models. We present a conceptual framework for selecting approaches that are best matched to the question of interest. We weigh the merits and limitations of each approach, survey the recent literature from diverse systems to quantify their use, and characterize the types of interactions being studied by each of them. We highlight the value of combining approaches and the importance of long-term data for establishing a baseline of phenological synchrony. Future work that scales up from pairwise species interactions to communities and ecosystems, emphasizing the use of predictive approaches, will be particularly valuable for reaching a broader understanding of the complex effects of climate change on the phenological overlap of interacting species. It will also be important to study a broader range of interactions: to date, most of the research on climate-induced phenological shifts has focused on terrestrial pairwise resource-consumer interactions, especially those between plants and insects.

Evolution of plant-pollinator mutualisms in response to climate change.

Climate change has the potential to desynchronize the phenologies of interdependent species, with potentially catastrophic effects on mutualist populations. Phenologies can evolve, but the role of evolution in the response of mutualisms to climate change is poorly understood. We developed a model that explicitly considers both the evolution and the population dynamics of a plant-pollinator mutualism under climate change. How the populations evolve, and thus whether the populations and the mutualism persist, depends not only on the rate of climate change but also on the densities and phenologies of other species in the community. Abundant alternative mutualist partners with broad temporal distributions can make a mutualism more robust to climate change, while abundant alternative partners with narrow temporal distributions can make a mutualism less robust. How community composition and the rate of climate change affect the persistence of mutualisms is mediated by two-species Allee thresholds. Understanding these thresholds will help researchers to identify those mutualisms at highest risk owing to climate change.