Predicting plant-pollinator interactions: concepts, methods, and challenges.

Plant-pollinator interactions are ecologically and economically important, and, as a result, their prediction is a crucial theoretical and applied goal for ecologists. Although various analytical methods are available, we still have a limited ability to predict plant-pollinator interactions. The predictive ability of different plant-pollinator interaction models depends on the specific definitions used to conceptualize and quantify species attributes (e.g., morphological traits), sampling effects (e.g., detection probabilities), and data resolution and availability. Progress in the study of plant-pollinator interactions requires conceptual and methodological advances concerning the mechanisms and species attributes governing interactions as well as improved modeling approaches to predict interactions. Current methods to predict plant-pollinator interactions present ample opportunities for improvement and spark new horizons for basic and applied research.

Genotype accounts for intraspecific variation in the timing and duration of multiple, sequential life-cycle events in a willow species.

PREMISE: Phenological variation among individuals within populations is common and has a variety of ecological and evolutionary consequences, including forming the basis for population-level responses to environmental change. Although the timing of life-cycle events has genetic underpinnings, whether intraspecific variation in the duration of life-cycle events reflects genetic differences among individuals is poorly understood. METHODS: We used a common garden experiment with 10 genotypes of Salix hookeriana (coastal willow) from northern California, United States to investigate the extent to which genetic variation explains intraspecific variation in the timing and duration of multiple, sequential life-cycle events: flowering, leaf budbreak, leaf expansion, fruiting, and fall leaf coloration. We used seven clones of each genotype, for a total of 70 individual trees. RESULTS: Genotype affected each sequential life-cycle event independently and explained on average 62% of the variation in the timing and duration of vegetative and reproductive life-cycle events. All events were significantly heritable. A single genotype tended to be "early" or "late" across life-cycle events, but for event durations, there was no consistent response within genotypes. CONCLUSIONS: This research demonstrates that genetic variation can be a major component underlying intraspecific variation in the timing and duration of life-cycle events. It is often assumed that the environment affects durations, but we show that genetic factors also play a role. Because the timing and duration of events are independent of one another, our results suggest that the effects of environmental change on one event will not necessarily cascade to subsequent events.

Ecological Drivers and Consequences of Bumble Bee Body Size Variation.

Body size is arguably one of the most important traits influencing the physiology and ecology of animals. Shifts in animal body size have been observed in response to climate change, including in bumble bees (Bombus spp. [Hymenoptera: Apidae]). Bumble bee size shifts have occurred concurrently with the precipitous population declines of several species, which appear to be related, in part, to their size. Body size variation is central to the ecology of bumble bees, from their social organization to the pollination services they provide to plants. If bumble bee size is shifted or constrained, there may be consequences for the pollination services they provide and for our ability to predict their responses to global change. Yet, there are still many aspects of the breadth and role of bumble bee body size variation that require more study. To this end, we review the current evidence of the ecological drivers of size variation in bumble bees and the consequences of that variation on bumble bee fitness, foraging, and species interactions. In total we review: (1) the proximate determinants and physiological consequences of size variation in bumble bees; (2) the environmental drivers and ecological consequences of size variation; and (3) synthesize our understanding of size variation in predicting how bumble bees will respond to future changes in climate and land use. As global change intensifies, a better understanding of the factors influencing the size distributions of bumble bees, and the consequences of those distributions, will allow us to better predict future responses of these pollinators.

The shifting importance of abiotic and biotic factors across the life cycles of wild pollinators.

Organisms living in seasonal environments are exposed to different environmental conditions as they transition from one life stage to the next across their life cycle. How different life stages respond to these varying conditions, and the extent to which different life stages are linked, are fundamental components of the ecology of an organism. Nevertheless, the influence of abiotic and biotic factors on different parts of an organism's life cycle is often not accounted for, which limits our understanding of the ecological consequences of environmental change. We investigated the relative importance of climate conditions, food availability, and previous life-stage abundance in an assemblage of seven wild bumble bee species, asking: how do these three factors directly influence bee abundance at each life stage? To do so, we used a 7-year dataset where we monitored climate conditions, floral resources, and abundances of bees in each life stage across the active colony life cycle in a highly seasonal subalpine ecosystem in the Colorado Rocky Mountains, USA. Bee abundance at different life stages responded to abiotic and biotic conditions in a broadly consistent manner across the seven species: the survival and recruitment stage of the life cycle (overwintered queens) responded negatively to longer winters; the growth stage (workers) responded positively to floral resource availability; and the reproductive stage (males) was positively related to the abundance of the previous life stage (workers). Most species also exhibited some idiosyncratic responses. Our long-term examination of annual bumble bees reveals a general set of responses in the abundance of each life stage to climate conditions, floral resource availability, and previous life stage. Across species, these three factors each directly influenced a distinct life stage, illustrating how their relative importance can shift throughout the life cycle. The life-cycle approach that we have taken highlights that important details about demography can be overlooked without considering life-stage-specific responses. Ultimately, it is these life-stage-specific responses that shape population outcomes, not only for animal pollinators but also for many organisms living in seasonal environments.

Reef fishes weaken dietary preferences after coral mortality, altering resource overlap.

The direct and indirect effects of climate change can affect, and are mediated by, changes in animal behaviour. However, we often lack sufficient empirical data to assess how large-scale disturbances affect the behaviour of individuals, which scales up to influence communities. Here, we investigate these patterns by focusing on the foraging behaviour of butterflyfishes, prominent coral-feeding fishes on coral reefs, before and after a mass coral bleaching event in Iriomote, Japan. In response to 65% coral mortality, coral-feeding fishes broadened their diets, showing a significant weakening of dietary preferences across species. Multiple species reduced their consumption of bleaching-sensitive Acropora corals, while expanding their diets to consume a variety of other coral genera. This resulted in decreased dietary overlap among butterflyfishes. Behavioural changes in response to bleaching may increase resilience of coral reef fishes in the short term. However, coral mortality has reduced populations of coral-feeders world-wide, indicating the changes in feeding behaviour we document here may not be sufficient to ensure long-term resilience of butterflyfishes on coral reefs.

Sodium-enriched floral nectar increases pollinator visitation rate and diversity.

Plants have evolved a variety of approaches to attract pollinators, including enriching their nectar with essential nutrients. Because sodium is an essential nutrient for pollinators, and sodium concentration in nectar can vary both within and among species, we explored whether experimentally enriching floral nectar with sodium in five plant species would influence pollinator visitation and diversity. We found that the number of visits by pollinators increased on plants with sodium-enriched nectar, regardless of plant species, relative to plants receiving control nectar. Similarly, the number of species visiting plants with sodium-enriched nectar was twice that of controls. Our findings suggest that sodium in floral nectar may play an important but unappreciated role in the ecology and evolution of plant-pollinator mutualisms.

Plant-pollinator interaction niche broadens in response to severe drought perturbations.

The composition of plant-pollinator interactions-i.e., who interacts with whom in diverse communities-is highly dynamic, and we have a very limited understanding of how interaction identities change in response to perturbations in nature. One prediction from niche and diet theory is that resource niches will broaden to compensate for resource reductions driven by perturbations, yet this has not been empirically tested in plant-pollinator systems in response to real-world perturbations in the field. Here, we use a long-term dataset of floral visitation to Ipomopsis aggregata, a montane perennial herb, to test whether the breadth of its floral visitation niche (i.e., flower visitor richness) changed in response to naturally occurring drought perturbations. Fewer floral resources are available in drought years, which could drive pollinators to expand their foraging niches, thereby expanding plants' floral visitation niches. We compared two drought years to three non-drought years to analyze changes in niche breadth and community composition of floral visitors to I. aggregata, predicting broadened niche breadth and distinct visitor community composition in drought years compared to non-drought years. We found statistically significant increases in niche breadth in drought years as compared to non-drought conditions, but no statistically distinguishable changes in community composition of flower visitors. Our findings suggest that plants' floral visitation niches may exhibit considerable plasticity in response to disturbance. This may have widespread consequences for community-level stability as well as functional consequences if increased niche overlap affects pollination services.

Seeing through the static: the temporal dimension of plant-animal mutualistic interactions.

Most studies of plant-animal mutualistic networks have come from a temporally static perspective. This approach has revealed general patterns in network structure, but limits our ability to understand the ecological and evolutionary processes that shape these networks and to predict the consequences of natural and human-driven disturbance on species interactions. We review the growing literature on temporal dynamics of plant-animal mutualistic networks including pollination, seed dispersal and ant defence mutualisms. We then discuss potential mechanisms underlying such variation in interactions, ranging from behavioural and physiological processes at the finest temporal scales to ecological and evolutionary processes at the broadest. We find that at the finest temporal scales (days, weeks, months) mutualistic interactions are highly dynamic, with considerable variation in network structure. At intermediate scales (years, decades), networks still exhibit high levels of temporal variation, but such variation appears to influence network properties only weakly. At the broadest temporal scales (many decades, centuries and beyond), continued shifts in interactions appear to reshape network structure, leading to dramatic community changes, including loss of species and function. Our review highlights the importance of considering the temporal dimension for understanding the ecology and evolution of complex webs of mutualistic interactions.

Untangling the seasonal dynamics of plant-pollinator communities.

Ecological communities often show changes in populations and their interactions over time. To date, however, it has been challenging to effectively untangle the mechanisms shaping such dynamics. One approach that has yet to be fully explored is to treat the varying structure of empirical communities-i.e. their network of interactions-as time series. Here, we follow this approach by applying a network-comparison technique to study the seasonal dynamics of plant-pollinator networks. We find that the structure of these networks is extremely variable, where species constantly change how they interact with each other within seasons. Most importantly, we find the holistic dynamic of plants and pollinators to be remarkably coherent across years, allowing us to reveal general rules by which species first enter, then change their roles, and finally leave the networks. Overall, our results disentangle key aspects of species' interaction turnover, phenology, and seasonal assembly/disassembly processes in empirical plant-pollinator communities.

Contrasting effects of climate change on seasonal survival of a hibernating mammal.

Seasonal environmental conditions shape the behavior and life history of virtually all organisms. Climate change is modifying these seasonal environmental conditions, which threatens to disrupt population dynamics. It is conceivable that climatic changes may be beneficial in one season but result in detrimental conditions in another because life-history strategies vary between these time periods. We analyzed the temporal trends in seasonal survival of yellow-bellied marmots (Marmota flaviventer) and explored the environmental drivers using a 40-y dataset from the Colorado Rocky Mountains (USA). Trends in survival revealed divergent seasonal patterns, which were similar across age-classes. Marmot survival declined during winter but generally increased during summer. Interestingly, different environmental factors appeared to drive survival trends across age-classes. Winter survival was largely driven by conditions during the preceding summer and the effect of continued climate change was likely to be mainly negative, whereas the likely outcome of continued climate change on summer survival was generally positive. This study illustrates that seasonal demographic responses need disentangling to accurately forecast the impacts of climate change on animal population dynamics.

Two-Year Bee, or Not Two-Year Bee? How Voltinism Is Affected by Temperature and Season Length in a High-Elevation Solitary Bee.

Organisms must often make developmental decisions without complete information about future conditions. This uncertainty-for example, about the duration of conditions favorable for growth-can favor bet-hedging strategies. Here, we investigated the causes of life cycle variation in Osmia iridis, a bee exhibiting a possible bet-hedging strategy with co-occurring 1- and 2-year life cycles. One-year bees reach adulthood quickly but die if they fail to complete pupation before winter; 2-year bees adopt a low-risk, low-reward strategy of postponing pupation until the second summer. We reared larval bees in incubators in various experimental conditions and found that warmer-but not longer-summers and early birthdates increased the frequency of 1-year life cycles. Using in situ temperature measurements and developmental trajectories of laboratory- and field-reared bees, we estimated degree-days required to reach adulthood in a single year. Local long-term (1950-2015) climate records reveal that this heat requirement is met in only ∼7% of summers, suggesting that the observed distribution of life cycles is adaptive. Warming summers will likely decrease average generation times in these populations. Nevertheless, survival of bees attempting 1-year life cycles-particularly those developing from late-laid eggs-will be <100%; consequently, we expect the life cycle polymorphism to persist.

Atypical Flowers Can Be as Profitable as Typical Hummingbird Flowers.

In western North America, hummingbirds can be observed systematically visiting flowers that lack the typical reddish color, tubular morphology, and dilute nectar of "hummingbird flowers." Curious about this behavior, we asked whether these atypical flowers are energetically profitable for hummingbirds. Our field measurements of nectar content and hummingbird foraging speeds, taken over four decades at multiple localities, show that atypical flowers can be as profitable as typical ones and suggest that the profit can support 24-h metabolic requirements of the birds. Thus, atypical flowers may contribute to successful migration of hummingbirds, enhance their population densities, and allow them to occupy areas seemingly depauperate in suitable resources. These results illustrate what can be gained by attending to the unexpected.

Interaction rewiring and the rapid turnover of plant-pollinator networks.

Whether species interactions are static or change over time has wide-reaching ecological and evolutionary consequences. However, species interaction networks are typically constructed from temporally aggregated interaction data, thereby implicitly assuming that interactions are fixed. This approach has advanced our understanding of communities, but it obscures the timescale at which interactions form (or dissolve) and the drivers and consequences of such dynamics. We address this knowledge gap by quantifying the within-season turnover of plant-pollinator interactions from weekly censuses across 3 years in a subalpine ecosystem. Week-to-week turnover of interactions (1) was high, (2) followed a consistent seasonal progression in all years of study and (3) was dominated by interaction rewiring (the reassembly of interactions among species). Simulation models revealed that species' phenologies and relative abundances constrained both total interaction turnover and rewiring. Our findings reveal the diversity of species interactions that may be missed when the temporal dynamics of networks are ignored.

Phenological responses to climate change do not exhibit phylogenetic signal in a subalpine plant community.

Phylogenetic relationships may underlie species-specific phenological sensitivities to abiotic variation and may help to predict these responses to climate change. Although shared evolutionary history may mediate both phenology and phenological sensitivity to abiotic variation, few studies have explicitly investigated whether this is the case. We explore phylogenetic signal in flowering phenology and in phenological sensitivity to temperature and snowmelt using a 39-year record of flowering from the Colorado Rocky Mountains, USA that includes dates of first, peak, and last flowering, and flowering duration for 60 plant species in a subalpine plant community. Consistent with other studies, we found evidence in support of phylogenetic signal in first flowering date. However, the strength and significance of that signal were inconsistent across other measures of flowering in this plant community: peak flowering date exhibited the strongest phylogenetic signal, followed by first flowering date; last flowering date and duration of flowering exhibited patterns indistinguishable from random trait evolution. In contrast to first and peak flowering date, phenological sensitivities of all flowering measures to temperature and snowmelt did not exhibit a phylogenetic signal. These findings show that within ecological communities, phylogenetic signal in phenology does not necessarily imply phylogenetic signal in phenological sensitivities to abiotic variation.

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.

Shifts in flowering phenology reshape a subalpine plant community.

Phenology--the timing of biological events--is highly sensitive to climate change. However, our general understanding of how phenology responds to climate change is based almost solely on incomplete assessments of phenology (such as first date of flowering) rather than on entire phenological distributions. Using a uniquely comprehensive 39-y flowering phenology dataset from the Colorado Rocky Mountains that contains more than 2 million flower counts, we reveal a diversity of species-level phenological shifts that bring into question the accuracy of previous estimates of long-term phenological change. For 60 species, we show that first, peak, and last flowering rarely shift uniformly and instead usually shift independently of one another, resulting in a diversity of phenological changes through time. Shifts in the timing of first flowering on average overestimate the magnitude of shifts in the timing of peak flowering, fail to predict shifts in the timing of last flowering, and underrepresent the number of species changing phenology in this plant community. Ultimately, this diversity of species-level phenological shifts contributes to altered coflowering patterns within the community, a redistribution of floral abundance across the season, and an expansion of the flowering season by more than I mo during the course of our study period. These results demonstrate the substantial reshaping of ecological communities that can be attributed to shifts in phenology.

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.

Asynchronous changes in phenology of migrating Broad-tailed Hummingbirds and their early-season nectar resources.

Phenological advancements driven by climate change are especially pronounced at higher latitudes, so that migrants from lower latitudes may increasingly arrive at breeding grounds after the appearance of seasonal resources. To explore this possibility, we compared dates of first arrival of Broad-tailed Hummingbirds (Selasphorus platycercus) to dates of flowering of plants they visit for nectar. Near the southern limit of the breeding range, neither hummingbird arrival nor first flowering dates have changed significantly over the past few decades. At a nearby migration stopover site, first flowering of a major food plant has advanced, but peak flowering has not. Near the northern limit of the breeding range, first and peak flowering of early-season food plants have shifted to earlier dates, resulting in a shorter interval between appearance of first hummingbirds and first flowers. If phenological shifts continue at current rates, hummingbirds will eventually arrive at northern breeding grounds after flowering begins, which could reduce their nesting success. These results support the prediction that migratory species may experience the greatest phenological mismatches at the poleward limits of their migration. A novel hypothesis based on these results posits that the poleward limit for some species may contract toward lower latitudes under continued warming.