Plant–pollinator interactions and phenological change: what can we learn about climate impacts from experiments and observations?

Climate change can affect plant–pollinator interactions in a variety of ways, but much of the research attention has focused on whether independent shifts in phenology will alter temporal overlap between plants and pollinators. Here I review the research on plant–pollinator mismatch, assessing the potential for observational and experimental approaches to address particular aspects of the problem. Recent, primarily observational studies suggest that phenologies of co‐occurring plants and pollinators tend to respond similarly to environmental cues, but that nevertheless, certain pairs of interacting species are showing independent shifts in phenology. Only in a few cases, however, have these independent shifts been shown to affect population vital rates (specifically, seed production by plants) but this largely reflects a lack of research. Compared to the few long‐term studies of pollination in natural plant populations, experimental manipulations of phenology have yielded relatively optimistic conclusions about effects of phenological shifts on plant reproduction, and I discuss how issues of scale and frequency‐dependence in pollinator behaviour affect the interpretation of these ‘temporal transplant’ experiments. Comparable research on the impacts of mismatch on pollinator populations is so far lacking, but both observational studies and focused experiments have the potential to improve our forecasts of pollinator responses to changing phenologies. Finally, while there is now evidence that plant–pollinator mismatch can affect seed production by plants, it is still unclear whether this phenological impact will be the primary way in which climate change affects plant–pollinator interactions. It would be useful to test the direct effects of changing climate on pollinator population persistence, and to compare the importance of phenological mismatch with other threats to pollination.     

Shifts in phenological distributions reshape interaction potential in natural communities

Climate change has changed the phenologies of species worldwide, but it remains unclear how these phenological changes will affect species interactions and the structure of natural communities. Using a novel approach to analyse long‐term data of 66 amphibian species pairs across eight communities, we demonstrate that phenological shifts can significantly alter the interaction potential of coexisting competitors. Importantly, these changes in interaction potential were mediated by non‐uniform, species‐specific shifts in entire phenological distributions and consequently could not be captured by metrics traditionally used to quantify phenological shifts. Ultimately, these non‐uniform shifts in phenological distributions increased the interaction potential for 25% of species pairs (and did not reduce interaction potential for any species pair), altering temporal community structure and potentially increasing interspecific competition. These results demonstrate the potential of phenological shifts to reshape temporal structure of natural communities, emphasising the importance of considering entire phenological distributions of natural populations.     

Foraging strategies of generalist and specialist Old World nectar bats in response to temporally variable floral resources

Foraging theory predicts that generalist foragers should switch resources more readily, while specialist foragers should remain constant to preferred food resources. Plant‐pollinator interactions provide a convenient system to test such predictions because floral resources are often temporally patchy, thus requiring long‐lived pollinators to switch resources seasonally. Furthermore, flowering phenologies range from ‘steady‐state’ (low‐rewarding but highly reliable) to ‘big‐bang’ (high‐rewarding but ephemeral) plant species. We assessed how nectarivorous Old World bats respond to this temporally variable floral environment by examining their diets throughout the year. Over 15 months of fieldwork in southern Thailand, we simultaneously: (1) recorded the flowering phenologies of six bat‐pollinated plant taxa; and (2) assessed the diets of seven common flower‐visiting bat species. As predicted, the generalist nectarivore (Eonycteris spelaea) frequently switched diets and utilized both big‐bang and steady‐state resources, while the specialist nectarivores (Macroglossus minimus and M. sobrinus) foraged on one or two steady‐state plant species year‐round. Our results suggest that larger and faster bat species are able to fly longer distances in search of big‐bang resources, while smaller bat species rely on highly predictable food resources. This study supports the theory that generalist foragers have flexible diets, while specialist species restrict foraging to preferred floral resources even when other floral resources are more abundant. Moreover, these findings demonstrate how plant flowering phenology and pollinator diet breadth can shape the frequency and constancy of pollinator visits; we further discuss how such interactions can influence the potential extent of gene flow within a patchy floral environment.     

Coexistence of plant species in a biodiversity hotspot is stabilized by competition but not by seed predation

Understanding the mechanisms of species coexistence is a key task for ecology. Recent theory predicts that both competition and predation (which causes apparent competition among prey) can either promote or limit species coexistence. Both mechanisms cause negative interactions between individuals, and each mechanism promotes stable coexistence if it causes negative interactions to be stronger between conspecifics than between heterospecifics. However, the relative importance of competition and predation for coexistence in natural communities is poorly known. Here, we study how competition and apparent competition via pre‐dispersal seed predators affect the long‐term fecundity of Protea shrubs in the fire‐prone Fynbos biome (South Africa). These shrubs store all viable seeds produced since the last fire in fire‐proof cones. Competitive effects on cone number and pre‐dispersal seed predation reduce their fecundity and can thus limit recruitment after the next fire. In 27 communities comprising 49 990 shrubs of 22 Protea species, we measured cone number and per‐cone seed predation rate of 2154 and 1755 focal individuals, respectively. Neighbourhood analyses related these measures to individual‐based community maps. We found that conspecific neighbours had stronger competitive effects on cone number than heterospecific neighbours. In contrast, apparent competition via seed predators was comparable between conspecifics and heterospecifics. This indicates that competition stabilizes coexistence of Protea species, whereas pre‐dispersal seed predation does not. Larger neighbours had stronger competitive effects and neighbours with large seed crops exerted stronger apparent competition. For 97% of the focal plants, competition reduced fecundity more than apparent competition. Our results show that even in communities of closely related and ecologically similar species, intraspecific competition can be stronger than interspecific competition. On the other hand, apparent competition through seed predators need not have such a stabilizing effect. These findings illustrate the potential of ‘community demography’, the demographic study of multiple interacting species, for understanding plant coexistence.     

Reconciling empirical interactions and species coexistence

Coexistence in ecological communities is governed largely by the nature and intensity of species interactions. Countless studies have proposed methods to infer these interactions from empirical data, yet models parameterised using such data often fail to recover observed coexistence patterns. Here, we propose a method to reconcile empirical parameterisations of community dynamics with species‐abundance data, ensuring that the predicted equilibrium is consistent with the observed abundance distribution. To illustrate the approach, we explore two case studies: an experimental freshwater algal community and a long‐term time series of displacement in an intertidal community. We demonstrate how our method helps recover observed coexistence patterns, capture the core dynamics of the system, and, in the latter case, predict the impacts of experimental extinctions. Collectively, these results demonstrate an intuitive approach for reconciling observed and empirical data, improving our ability to explore the links between species interactions and coexistence in natural systems.     

Predicting future coexistence in a North American ant community

Global climate change will remodel ecological communities worldwide. However, as a consequence of biotic interactions, communities may respond to climate change in idiosyncratic ways. This makes predictive models that incorporate biotic interactions necessary. We show how such models can be constructed based on empirical studies in combination with predictions or assumptions regarding the abiotic consequences of climate change. Specifically, we consider a well‐studied ant community in North America. First, we use historical data to parameterize a basic model for species coexistence. Using this model, we determine the importance of various factors, including thermal niches, food discovery rates, and food removal rates, to historical species coexistence. We then extend the model to predict how the community will restructure in response to several climate‐related changes, such as increased temperature, shifts in species phenology, and altered resource availability. Interestingly, our mechanistic model suggests that increased temperature and shifts in species phenology can have contrasting effects. Nevertheless, for almost all scenarios considered, we find that the most subordinate ant species suffers most as a result of climate change. More generally, our analysis shows that community composition can respond to climate warming in nonintuitive ways. For example, in the context of a community, it is not necessarily the most heat‐sensitive species that are most at risk. Our results demonstrate how models that account for niche partitioning and interspecific trade‐offs among species can be used to predict the likely idiosyncratic responses of local communities to climate change.     

Disentangling climate change effects on species interactions: effects of temperature, phenological shifts, and body size

Climate-mediated shifts in species’ phenologies are expected to alter species interactions, but predicting the consequences of this is difficult because phenological shifts may be driven by different climate factors that may or may not be correlated. Temperature could be an important factor determining effects of phenological shifts by altering species’ growth rates and thereby the relative size ratios of interacting species. We tested this hypothesis by independently manipulating temperature and the relative hatching phenologies of two competing amphibian species. Relative shifts in hatching time generally altered the strength of competition, but the presence and magnitude of this effect was temperature dependent and joint effects of temperature and hatching phenology were non-additive. Species that hatched relatively early or late performed significantly better or worse, respectively, but only at higher temperatures and not at lower temperatures. As a consequence, climate-mediated shifts in hatching phenology or temperature resulted in stronger or weaker effects than expected when both factors acted in concert. Furthermore, consequences of phenological shifts were asymmetric; arriving relatively early had disproportional stronger (or weaker) effects than arriving relatively late, and this varied with species identity. However, consistent with recent theory, these seemingly idiosyncratic effects of phenological shifts could be explained by species-specific differences in growth rates across temperatures and concordant shifts in relative body size of interacting species. Our results emphasize the need to account for environmental conditions when predicting the effects of phenological shifts, and suggest that shifts in size-structured interactions can mediate the impact of climate change on natural communities.     

结构稳定性: 概念、方法和应用

群落内物种间相互作用的结构是高度组织化的。群落结构对多物种共存的影响机制是群落生态学的核心科学问题之一。目前生态学界在这一问题上存在多种不同的观点。一个可能的原因是, 由于环境因子的复杂性, 大部分研究忽略了环境因子对群落结构和物种共存的重要影响。在这一背景下, 近期发展起来的结构稳定性理论系统地联系了群落结构、环境因子和物种共存, 并在此基础上建立了一个和经验数据紧密结合的理论框架。本文首先简要回顾了当前关于群落结构研究的争鸣, 然后介绍了结构稳定性的理论框架和计算方法, 最后详细介绍了结构稳定性理论在不同生态群落和不同生态学问题中的应用。在全球气候变化的背景下, 结构稳定性理论提供了一种新的视角来理解群落层面的生物多样性维持机制。     

Potential mechanisms of coexistence in closely related forbs

The stable coexistence of very similar species has perplexed ecologists for decades and has been central to the development of coexistence theory. According to modern coexistence theory, species can coexist stably (i.e. persist indefinitely with no long‐term density trends) as long as species' niche differences exceed competitive ability differences, even if these differences are very small. Recent studies have directly quantified niche and competitive ability differences in experimental communities at small spatial scales, but provide limited information about stable coexistence across spatial scales in heterogeneous natural communities. In this study, we use experimental and observational approaches to explore evidence for niche and competitive ability differences between two closely related, ecologically similar and widely coexisting annual forbs: Trachymene cyanopetala and T. ornata. We experimentally tested for stabilizing niche differences and competitive ability differences between these species by manipulating species' frequencies, under both well‐watered and water‐stressed conditions. We considered these experimental results in light of extensive field observations to explore evidence of niche segregation at a range of spatial scales. We found little evidence of intra‐specific stabilization or competitive ability differences in laboratory experiments while observational studies suggested niche segregation across pollinator assemblages and small‐scale microclimate heterogeneity. Though we did not quantify long‐term stabilization of coexisting populations of these species, results are consistent with expectations for stable coexistence of similar species via a spatial storage effect allowing niche differences to overcome even small (to absent) competitive ability differences.     

Combining field experiments and individual-based modeling to identify the dynamically relevant organizational scale in a field system

Community ecologists continually strive to build analytical models that realistically describe long‐term dynamics of the systems they study. A key step in this process is identifying which details are relevant for predicting dynamics. Currently, this remains a limiting step in development of analytical theory because experimental field ecology, which provides the key empirical insight, and theoretical ecology, which translates empirical knowledge into analytical theory, remain weakly linked. I illustrate how an individual‐based computational model of species interactions is a useful way to bridge the gulf between empirical research and theory development. I built a computational model that reproduced key natural history and biological detail of an old‐field interaction web composed of a predator species, a herbivore species and two plant groups that had been the subject of extensive previous field research. I examined, using simulation experiments, how individual behavior of herbivores in response to changing resource and predator abundance scaled to long‐term population‐level and community‐level dynamics. The simulation experiments revealed that the long‐term community dynamics could be highly predictable because of two counterintuitive reasons. First, seasonality was a strong forcing variable on the system that removed the possibility of serial dependence in population abundance over time. Second, because of seasonality, short‐term behavioral responses of herbivores played a much stronger role in shaping community structure than longer‐term processes such as density responses. So, simply knowing the short‐term responses of herbivores at the evolutionary ecological level was sufficient to forecast the long‐term outcome of experimental manipulations. This study shows that an individual‐based model, once it is calibrated to the real‐world field system, can provide key insight into the biological detail that analytical models should include to predict long‐term dynamics.     

Are all intertidal wetlands naturally created equal? Bottlenecks,thresholds and knowledge gaps to mangrove and saltmarsh ecosystems

Intertidal wetlands such as saltmarshes and mangroves provide numerous important ecological functions, though they are in rapid and global decline. To better conserve and restore these wetland ecosystems, we need an understanding of the fundamental natural bottlenecks and thresholds to their establishment and long‐term ecological maintenance. Despite inhabiting similar intertidal positions, the biological traits of these systems differ markedly in structure, phenology, life history, phylogeny and dispersal, suggesting large differences in biophysical interactions. By providing the first systematic comparison between saltmarshes and mangroves, we unravel how the interplay between species‐specific life‐history traits, biophysical interactions and biogeomorphological feedback processes determine where, when and what wetland can establish, the thresholds to long‐term ecosystem stability, and constraints to genetic connectivity between intertidal wetland populations at the landscape level. To understand these process interactions, research into the constraints to wetland development, and biological adaptations to overcome these critical bottlenecks and thresholds requires a truly interdisciplinary approach.     

Trait matching and phenological overlap increase the spatio‐temporal stability and functionality of plant–pollinator interactions

Morphology and phenology influence plant–pollinator network structure, but whether they generate more stable pairwise interactions with higher pollination success remains unknown. Here we evaluate the importance of morphological trait matching, phenological overlap and specialisation for the spatio‐temporal stability (measured as variability) of plant–pollinator interactions and for pollination success, while controlling for species' abundance. To this end, we combined a 6‐year plant–pollinator interaction dataset, with information on species traits, phenologies, specialisation, abundance and pollination success, into structural equation models. Interactions among abundant plants and pollinators with well‐matched traits and phenologies formed the stable and functional backbone of the pollination network, whereas poorly matched interactions were variable in time and had lower pollination success. We conclude that phenological overlap could be more useful for predicting changes in species interactions than species abundances, and that non‐random extinction of species with well‐matched traits could decrease the stability of interactions within communities and reduce their functioning.     

A spatial theory for emergent multiple predator–prey interactions in food webs

Predator–prey interaction is inherently spatial because animals move through landscapes to search for and consume food resources and to avoid being consumed by other species. The spatial nature of species interactions necessitates integrating spatial processes into food web theory and evaluating how predators combine to impact their prey. Here, we present a spatial modeling approach that examines emergent multiple predator effects on prey within landscapes. The modeling is inspired by the habitat domain concept derived from empirical synthesis of spatial movement and interactions studies. Because these principles are motivated by synthesis of short‐term experiments, it remains uncertain whether spatial contingency principles hold in dynamical systems. We address this uncertainty by formulating dynamical systems models, guided by core habitat domain principles, to examine long‐term multiple predator–prey spatial dynamics. To describe habitat domains, we use classical niche concepts describing resource utilization distributions, and assume species interactions emerge from the degree of overlap between species. The analytical results generally align with those from empirical synthesis and present a theoretical framework capable of demonstrating multiple predator effects that does not depend on the small spatial or temporal scales typical of mesocosm experiments, and help bridge between empirical experiments and long‐term dynamics in natural systems.     

Impacts of consumer–resource interaction transitions on persistence and long‐term interaction outcomes of random ecological networks

Despite the prevalence of context‐dependent interaction transitions in ecological systems, their impacts on persistence and interaction diversity have scarcely been explored in complex ecological networks. By using multispecies bi‐directional and unidirectional consumer–resource models, representing a continuum of interaction transitions (sign change of interaction outcomes), we investigated the effects of structural interaction transitions on persistence (the fraction of remaining species) and long‐term interaction outcomes in random ecological networks. We found that high interaction strength of exploiting resources generally decreased persistence, and high strength of providing resources increased persistence when the strength of exploiting resources was low in more complex networks; also, the networks with high persistence had a high proportion of mutualistic interactions relative to antagonistic interactions present initially and over the long term. The shifting of interaction strengths shaped the long‐term interaction compositions. Meanwhile, population dynamics, especially species extinction, affected the difference between initial and long‐term interactions. Based on classical consumer–resource theory, these results establish a transitional continuum of interaction outcomes in ecological networks and imply a theoretical association among interaction transition, community persistence and interaction diversity.     

Predicting phenology by integrating ecology,evolution and climate science

Forecasting how species and ecosystems will respond to climate change has been a major aim of ecology in recent years. Much of this research has focused on phenology – the timing of life‐history events. Phenology has well‐demonstrated links to climate, from genetic to landscape scales; yet our ability to explain and predict variation in phenology across species, habitats and time remains poor. Here, we outline how merging approaches from ecology, climate science and evolutionary biology can advance research on phenological responses to climate variability. Using insight into seasonal and interannual climate variability combined with niche theory and community phylogenetics, we develop a predictive approach for species’ reponses to changing climate. Our approach predicts that species occupying higher latitudes or the early growing season should be most sensitive to climate and have the most phylogenetically conserved phenologies. We further predict that temperate species will respond to climate change by shifting in time, while tropical species will respond by shifting space, or by evolving. Although we focus here on plant phenology, our approach is broadly applicable to ecological research of plant responses to climate variability.     

(A bit) Earlier or later is always better: Phenological shifts in consumer–resource interactions

Phenology is a crucial life history trait for species interactions and it can have great repercussions on the persistence of communities and ecosystems. Changes in phenology caused by climate change can disrupt species interactions causing decreases in consumer growth rates, as suggested by the match–mismatch hypothesis (MMH). However, it is still not clear what the long-term consequences of such phenological changes are. In this paper, we present models in which phenology and consumer–resource feedbacks determine long-term community dynamics. Our results show that consumer viability is constrained by limits in the amount of phenological mismatch with their resources, in accordance with the MMH, but the effects of phenological shifts are often nonmonotonic. Consumers generally have higher abundances when they recruit some time before or after their resources because this reduces the long-term effects of overexploitation that would otherwise occur under closer synchrony. Changes in the duration of recruitment phenologies also have important impacts on community stability, with shorter phenologies promoting oscillations and cycles. For small community modules, the effects of phenological shifts on populations can be explained, to a great extent, as superpositions of their effects on consumer–resource pairs. We highlight that consumer–resource feedbacks and overexploitation, which are not typically considered in phenological models, are important factors shaping the long-term responses to phenological changes caused by climate change.     

Quantifying the relative importance of variation in predation and the environment for species coexistence

Coexistence and food web theory are two cornerstones of the long‐standing effort to understand how species coexist. Although competition and predation are known to act simultaneously in communities, theory and empirical study of these processes continue to be developed largely independently. Here, we integrate modern coexistence theory and food web theory to simultaneously quantify the relative importance of predation and environmental fluctuations for species coexistence. We first examine coexistence in a theoretical, multitrophic model, adding complexity to the food web using machine learning approaches. We then apply our framework to a stochastic model of the rocky intertidal food web, partitioning empirical coexistence dynamics. We find the main effects of both environmental fluctuations and variation in predator abundances contribute substantially to species coexistence. Unexpectedly, their interaction tends to destabilise coexistence, leading to new insights about the role of bottom‐up vs. top‐down forces in both theory and the rocky intertidal ecosystem.     

Phenology, ontogeny and the effects of climate change on the timing of species interactions

Climate change is altering the phenology of many species and the timing of their interactions with other species, but the impacts of these phenological shifts on species interactions remain unclear. Classical approaches to the study of phenology have typically documented changes in the timing of single life-history events, while phenological shifts affect many interactions over entire life histories. In this study, we suggest an approach that integrates the phenology and ontogeny of species interactions with a fitness landscape to provide a common mechanistic framework for investigating phenological shifts. We suggest that this ontogeny–phenology landscape provides a flexible method to document changes in the relative phenologies of interacting species, examine the causes of these phenological shifts, and estimate their consequences for interacting species.
Ecology Letters (2010) 13: 1–10     

Sugar landscapes and pollinator‐mediated interactions in plant communities

Pollinator‐mediated interactions between plants can play an important role for the dynamics of plant communities. Pollination services depend on the abundance and the foraging behaviour of pollinators, which in turn respond to the availability and distribution of floral resources (notably nectar sugar). However, it is still insufficiently understood how the ‘sugar landscapes’ provided by flowering plant communities shape pollinator‐mediated interactions between multiple plant species and across different spatial scales. A better understanding of pollinator‐mediated interactions requires an integrative approach that quantifies different aspects of sugar landscapes and investigates their relative importance for pollinator behaviour and plant reproductive success. In this study, we quantified such sugar landscapes from individual‐based maps of Protea shrub communities in the Cape Floristic Region, South Africa. The 27 study sites of 4 ha each jointly comprise 127 993 individuals of 19 species. We analysed how rates of visitation by key bird pollinators and the seed set of plants respond to different aspects of sugar landscapes: the distribution of nectar sugar amounts, as well as their quality, taxonomic purity and phenology. We found that pollinator visitation rates strongly depended on phenological variation of site‐scale sugar amounts. The seed set of focal plants increased with nectar sugar amounts of conspecific neighbours and with site‐scale sugar amounts. Seed set increased particularly strongly if site‐scale sugar amounts were provided by plants that offer less sugar per inflorescence. These combined effects of the amount, quality, purity and phenological variation of nectar sugar show that nectar sugar is a common interaction currency that determines how multiple plant species interact via shared pollinators. The responses of pollinator‐mediated interactions to different aspects of this interaction currency alter conditions for species coexistence in Protea communities and may cause community‐level Allee effects that promote extinction cascades.     

Dispersal-induced desynchronization: from metapopulations to metacommunities

The conceptualization of fragmented populations in terms of metapopulation theory has become standard over the last three decades. It is well known that increases in between‐patch migration rates cause more synchronous population fluctuations and that this coherence increases the risk of global metapopulation extinction. Because species’ migration rates and the probability of individuals surviving migration events depend on the effective distance between patches, the benefit of improving conservation corridors or the matrix between habitat patches has been questioned. As populations occur in the context of larger communities, moving from a metapopulation to a metacommunity model framework is a natural extension to address the generality of these conclusions. We show how considering a metacommunity can modify the conclusion that decreasing the effective distance between habitat patches (via improving matrix quality or other measures) necessarily increases the degree of metapopulation synchrony. We show that decreases in effective between‐patch distance may deter population synchrony because of the simultaneous effect this change has on the migration patterns of other species. These results indicate that species interactions need to be considered when the effect of conservation measures on population synchrony, and ultimately persistence, is addressed.