Laura A. Burkle

The future of plant-pollinator diversity: understanding interaction networks across time, space, and global change.

Structural analysis of plant-pollinator networks has revealed remarkably high species and interaction diversity and highlighted the species important for pollination services. Although techniques to analyze plant-pollinator networks began to emerge a decade ago, the characterization of spatiotemporal variation of interactions is still in its infancy. Understanding the ecological and evolutionary causes and consequences of spatial and temporal variation in plant-pollinator interactions is important for both basic and applied questions in community structure and function, the evolution of floral traits, and the development of optimal conservation strategies. Here we review observational, theoretical, and experimental studies of temporal and spatial variation in plant-pollinator interaction networks to establish a foundation for future studies to incorporate perspectives in spatiotemporal variation. Such perspectives are crucial given the rapid environmental changes associated with habitat loss, climate change, and biological invasions, which we discuss in this context. The inherent plasticity of plant-pollinator interactions and network structure suggests that many species should be able to persist by responding to environmental changes quickly, even though the identity of their mutualistic partners may change.

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.

Predicting the effects of nectar robbing on plant reproduction: implications of pollen limitation and plant mating system

The outcome of species interactions is often difficult to predict, depending on the organisms involved and the ecological context. Nectar robbers remove nectar from flowers, often without providing pollination service, and their effects on plant reproduction vary in strength and direction. In two case studies and a meta-analysis, we tested the importance of pollen limitation and plant mating system in predicting the impacts of nectar robbing on female plant reproduction. We predicted that nectar robbing would have the strongest effects on species requiring pollinators to set seed and pollen limited for seed production. Our predictions were partially supported. In the first study, natural nectar robbing was associated with lower seed production in Delphinium nuttallianum, a self-compatible but non-autogamously selfing, pollen-limited perennial, and experimental nectar robbing reduced seed set relative to unrobbed plants. The second study involved Linaria vulgaris, a self-incompatible perennial that is generally not pollen limited. Natural levels of nectar robbing generally had little effect on estimates of female reproduction in L. vulgaris, while experimental nectar robbing reduced seed set per fruit but not percentage of fruit set. A meta-analysis revealed that nectar robbing had strong negative effects on pollen-limited and self-incompatible plants, as predicted. Our results suggest that pollination biology and plant mating system must be considered to understand and predict the ecological outcome of both mutualistic and antagonistic plant-animal interactions.

Partitioning interaction turnover among alpine pollination networks: spatial, temporal, and environmental patterns

Ecologists have taken two distinct approaches in studying the distribution and diversity of communities: a species-centric focus and an interaction-network based approach. A current frontier in community-level studies is the integration of these perspectives by investigating both simultaneously; one method for achieving this is evaluating the relative contributions of species turnover and host switching towards interaction turnover (i.e., the dissimilarity in interactions between two networks). We performed observations of plant-pollinator interactions to investigate (1) patterns in interaction turnover across spatial, temporal, and environmental gradients and (2) the relative contribution of pollinator species turnover, floral turnover, simultaneous pollinator & floral turnover, and host switching towards interaction turnover. Field work was conducted on the Beartooth Plateau, an alpine ecosystem in Montana and Wyoming, with weekly observations of plant-pollinator interactions across one growing season. Interaction turnover increased through time, with magnitudes consistently greater than 80%, even at time intervals as short as one week. Floral species turnover (41%) and simultaneous floral and pollinator species turnover (36%) accounted for almost all interaction turnover while host switching accounted for only 5%. Interaction turnover also significantly increased with spatial and elevational distance, albeit with lesser magnitudes than with temporal distance. The marginal spatial pattern was present for only some taxa (Bombus spp. and solitary bee species), potentially indicating variable habitat use by pollinators across the landscape. Weak environmental trends may be a consequence of unmeasured environmental variables, yet our finding that environmental gradients structure plant-pollinator interaction partitions had not previously been tested with empirical data. Our observations suggest that host switching does not readily occur at the scales of alpine flowering phenology (i.e., ∼1 week); however, whether lack of host switching is indicative of inflexible pollinator foraging, or, more likely, a lack of opportunity or necessity to switch hosts, requires further investigation.

Shifts in pollinator composition and behavior cause slow interaction accumulation with area in plant–pollinator networks

Although ecologists have a solid understanding of the positive species-area relationship, little is known about how and why variation in habitat area influences the richness, structure, and function of species interaction networks. To address this, we investigated plant-pollinator interaction networks of the herbaceous rocky outcrop communities in Ozark glades (Missouri, USA) of different areas. We quantified the degree to which the increase in the number of species interactions with area differed from a null model based on sampling, where numbers of individuals increase with area. Although plant-pollinator interactions were expected to increase more steeply with area than species richness as a result of sampling, the observed rate of increase was considerably lower than expected. Two mechanisms could lead to this pattern: a higher proportion of specialist species in larger glades or generalist pollinators becoming more selective in their diets in larger glades. We found support for the former hypothesis, and those changes in species composition were strong enough to outweigh behavioral changes in the opposite direction; generalist pollinators were more selective in smaller glades. If these results are general, larger habitats may be needed to conserve interactions than would be thought based on species accumulation curves.

Drought and leaf herbivory influence floral volatiles and pollinator attraction

The effects of climate change on species interactions are poorly understood. Investigating the mechanisms by which species interactions may shift under altered environmental conditions will help form a more predictive understanding of such shifts. In particular, components of climate change have the potential to strongly influence floral volatile organic compounds (VOCs) and, in turn, plant-pollinator interactions. In this study, we experimentally manipulated drought and herbivory for four forb species to determine effects of these treatments and their interactions on (1) visual plant traits traditionally associated with pollinator attraction, (2) floral VOCs, and (3) the visitation rates and community composition of pollinators. For all forbs tested, experimental drought universally reduced flower size and floral display, but there were species-specific effects of drought on volatile emissions per flower, the composition of compounds produced, and subsequent pollinator visitation rates. Moreover, the community of pollinating visitors was influenced by drought across forb species (i.e. some pollinator species were deterred by drought while others were attracted). Together, these results indicate that VOCs may provide more nuanced information to potential floral visitors and may be relatively more important than visual traits for pollinator attraction, particularly under shifting environmental conditions.

Wildfire disturbance and productivity as drivers of plant species diversity across spatial scales

Wildfires influence many temperate terrestrial ecosystems worldwide. Historical environmental heterogeneity created by wildfires has been altered by human activities and will be impacted by future climate change. Our ability to predict the impact of wildfire-created heterogeneity on biodiversity is limited because few studies have investigated variation in community composition (beta-diversity) in response to fire. Wildfires may influence beta-diversity through several ecological mechanisms. First, high-severity fires may decrease beta-diversity by homogenizing species composition when they create landscapes dominated by disturbance-tolerant or rapidly colonizing species. In contrast, mixed-severity fires may increase beta-diversity by creating mosaic landscapes containing habitats that support species with differing environmental tolerances and dispersal traits. Moreover, the effects of fire severity on beta-diversity may change depending on site conditions. Disturbance is hypothesized to increase local species richness at higher productivity and decrease local species richness at lower productivity, a process that can have important, but largely unexamined, consequences on beta-diversity in fire-prone ecosystems. We tested these hypotheses by comparing patterns of beta-diversity and species richness across 162 plant communities in three sites that span a large-scale gradient in climate and productivity in the Northern Rockies of Montana. Within each site, we used spatially explicit fire-severity data to stratify sampling across unburned forests and forests burned with mixed- and high-severity wildfires. We found that beta-diversity (community dispersion) of forbs was higher in mixed-severity compared to high-severity fire, regardless of productivity. Counter to our predictions, local species richness of forbs was higher in burned landscapes compared to unburned landscapes at the low-productivity site, but lower in burned landscapes at the high-productivity site. This pattern may be explained by rapid regeneration of woody plants after fire in high-productivity forests. Moreover, forbs and woody plants had disproportionately higher overall species richness in mixed-severity fire compared to high-severity fire, but only at the low-productivity site. These patterns suggest that mixed-severity fires promote higher landscape-level biodiversity in low-productivity sites by increasing species turnover across landscapes with a diverse mosaic of habitats. Our study illustrates the importance of understanding the mechanisms by which patterns of wildfire severity interact with environmental gradients to influence patterns of biodiversity across spatial scales.

The beta-diversity of species interactions: Untangling the drivers of geographic variation in plant-pollinator diversity and function across scales.

PREMISE OF THE STUDY Geographic patterns of biodiversity have long inspired interest in processes that shape the assembly, diversity, and dynamics of communities at different spatial scales. To study mechanisms of community assembly, ecologists often compare spatial variation in community composition (beta-diversity) across environmental and spatial gradients. These same patterns inspired evolutionary biologists to investigate how micro- and macro-evolutionary processes create gradients in biodiversity. Central to these perspectives are species interactions, which contribute to community assembly and geographic variation in evolutionary processes. However, studies of beta-diversity have predominantly focused on single trophic levels, resulting in gaps in our understanding of variation in species-interaction networks (interaction beta-diversity), especially at scales most relevant to evolutionary studies of geographic variation. METHODS We outline two challenges and their consequences in scaling-up studies of interaction beta-diversity from local to biogeographic scales using plant-pollinator interactions as a model system in ecology, evolution, and conservation. KEY RESULTS First, we highlight how variation in regional species pools may contribute to variation in interaction beta-diversity among biogeographic regions with dissimilar evolutionary history. Second, we highlight how pollinator behavior (host-switching) links ecological networks to geographic patterns of plant-pollinator interactions and evolutionary processes. Third, we outline key unanswered questions regarding the role of geographic variation in plant-pollinator interactions for conservation and ecosystem services (pollination) in changing environments. CONCLUSIONS We conclude that the largest advances in the burgeoning field of interaction beta-diversity will come from studies that integrate frameworks in ecology, evolution, and conservation to understand the causes and consequences of interaction beta-diversity across scales.

Plant genotype, nutrients, and G × E interactions structure floral visitor communities

Intraspecific variation in plants is driven by both genetic and environmental factors and has been shown to play an important role in determining assemblages of herbivores, predators, and pathogens. Yet, the consequences of genetic (G) and environmental (E) factors, as well as potential (G × E) interactions, for floral visitor communities remains poorly explored. In a common garden experiment, we compared the relative effects of host-plant genotype and genotypic diversity as well as soil nutrient enrichment on floral resource abundance and insect floral visitors associated with tall goldenrod, Solidago altissima. We found that the floral visitor community varied considerably among genotypes, driven predominantly by variation in floral phenology among S. altissima clones. Floral visitors also varied among nutrient treatments, though this response was much weaker than to different plant genotypes, and was likely driven by effects of floral rewards rather than of floral phenology. Importantly, we also detected several G × E interactions for both flowering and floral visitors. Taken together, our results suggest that the effects of host-plant genetic variation, and to a lesser extent G × E interactions, are key agents in structuring the diversity and composition of floral visitors.

Effects of an invasive plant transcend ecosystem boundaries through a dragonfly-mediated trophic pathway.

Trophic interactions can strongly influence the structure and function of terrestrial and aquatic communities through top-down and bottom-up processes. Species with life stages in both terrestrial and aquatic systems may be particularly likely to link the effects of trophic interactions across ecosystem boundaries. Using experimental wetlands planted with purple loosestrife (Lythrum salicaria), we tested the degree to which the bottom-up effects of floral density of this invasive plant could trigger a chain of interactions, changing the behavior of terrestrial flying insect prey and predators and ultimately cascading through top-down interactions to alter lower trophic levels in the aquatic community. The results of our experiment support the linkage of terrestrial and aquatic food webs through this hypothesized pathway, with high loosestrife floral density treatments attracting high levels of visiting insect pollinators and predatory adult dragonflies. High floral densities were also associated with increased adult dragonfly oviposition and subsequently high larval dragonfly abundance in the aquatic community. Finally, high-flower treatments were coupled with changes in zooplankton species richness and shifts in the composition of zooplankton communities. Through changes in animal behavior and trophic interactions in terrestrial and aquatic systems, this work illustrates the broad and potentially cryptic effects of invasive species, and provides additional compelling motivation for ecologists to conduct investigations that cross traditional ecosystem boundaries.