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.     

Maintenance of temporal synchrony between syrphid flies and floral resources despite differential phenological responses to climate

Variation in species’ responses to abiotic phenological cues under climate change may cause changes in temporal overlap among interacting taxa, with potential demographic consequences. Here, we examine associations between the abiotic environment and plant–pollinator phenological synchrony using a long‐term syrphid fly–flowering phenology dataset (1992–2011). Degree‐days above freezing, precipitation, and timing of snow melt were investigated as predictors of phenology. Syrphids generally emerge after flowering onset and end their activity before the end of flowering. Neither flowering nor syrphid phenology has changed significantly over our 20‐year record, consistent with a lack of directional change in climate variables over the same time frame. Instead we document interannual variability in the abiotic environment and phenology. Timing of snow melt was the best predictor of flowering onset and syrphid emergence. Snow melt and degree‐days were the best predictors of the end of flowering, whereas degree‐days and precipitation best predicted the end of the syrphid period. Flowering advanced at a faster rate than syrphids in response to both advancing snow melt and increasing temperature. Different rates of phenological advancements resulted in more days of temporal overlap between the flower–syrphid community in years of early snow melt because of extended activity periods. Phenological synchrony at the community level is therefore likely to be maintained for some time, even under advancing snow melt conditions that are evident over longer term records at our site. These results show that interacting taxa may respond to different phenological cues and to the same cues at different rates but still maintain phenological synchrony over a range of abiotic conditions. However, our results also indicate that some individual plant species may overlap with the syrphid community for fewer days under continued climate change. This highlights the role of interannual variation in these flower–syrphid interactions and shows that species‐level responses can differ from community‐level responses in nonintuitive ways.     

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.     

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

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

A perspective on match/mismatch of phenology in community contexts

Climate change has significant impacts on phenology of various organisms in a species‐specific manner. Facing this problem, the match/mismatch hypothesis that phenological (a)synchrony with resource availability strongly influences recruitment success of a consumer population has recently received much attention. In this article, we discuss extending the conventional pairwise concept and demonstrate a community module‐based approach as an initial step for exploring community consequences of species‐specific phenological shifts caused by climate change. Our multispecies match/mismatch perspective leads to the prediction that phenological (a)synchrony among interacting species critically affects not only population recruitment of species but also key dynamical features of ecological communities such as trophic cascades, competitive hierarchies, and species coexistence. Explicit identification and consideration of species relationships is therefore desirable for a better understanding of seasonal community dynamics and thus community consequences of climate change‐induced phenological shifts.     

Species interactions and climate change: How the disruption of species co‐occurrence will impact on an avian forest guild

Interspecific interactions are crucial in determining species occurrence and community assembly. Understanding these interactions is thus essential for correctly predicting species' responses to climate change. We focussed on an avian forest guild of four hole‐nesting species with differing sensitivities to climate that show a range of well‐understood reciprocal interactions, including facilitation, competition and predation. We modelled the potential distributions of black woodpecker and boreal, tawny and Ural owl, and tested whether the spatial patterns of the more widespread species (excluding Ural owl) were shaped by interspecific interactions. We then modelled the potential future distributions of all four species, evaluating how the predicted changes will alter the overlap between the species' ranges, and hence the spatial outcomes of interactions. Forest cover/type and climate were important determinants of habitat suitability for all species. Field data analysed with N‐mixture models revealed effects of interspecific interactions on current species abundance, especially in boreal owl (positive effects of black woodpecker, negative effects of tawny owl). Climate change will impact the assemblage both at species and guild levels, as the potential area of range overlap, relevant for species interactions, will change in both proportion and extent in the future. Boreal owl, the most climate‐sensitive species in the guild, will retreat, and the range overlap with its main predator, tawny owl, will increase in the remaining suitable area: climate change will thus impact on boreal owl both directly and indirectly. Climate change will cause the geographical alteration or disruption of species interaction networks, with different consequences for the species belonging to the guild and a likely spatial increase of competition and/or intraguild predation. Our work shows significant interactions and important potential changes in the overlap of areas suitable for the interacting species, which reinforce the importance of including relevant biotic interactions in predictive climate change models for increasing forecast accuracy.     

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.     

Range position and climate sensitivity: The structure of among‐population demographic responses to climatic variation

Species’ distributions will respond to climate change based on the relationship between local demographic processes and climate and how this relationship varies based on range position. A rarely tested demographic prediction is that populations at the extremes of a species’ climate envelope (e.g., populations in areas with the highest mean annual temperature) will be most sensitive to local shifts in climate (i.e., warming). We tested this prediction using a dynamic species distribution model linking demographic rates to variation in temperature and precipitation for wood frogs (Lithobates sylvaticus) in North America. Using long‐term monitoring data from 746 populations in 27 study areas, we determined how climatic variation affected population growth rates and how these relationships varied with respect to long‐term climate. Some models supported the predicted pattern, with negative effects of extreme summer temperatures in hotter areas and positive effects on recruitment for summer water availability in drier areas. We also found evidence of interacting temperature and precipitation influencing population size, such as extreme heat having less of a negative effect in wetter areas. Other results were contrary to predictions, such as positive effects of summer water availability in wetter parts of the range and positive responses to winter warming especially in milder areas. In general, we found wood frogs were more sensitive to changes in temperature or temperature interacting with precipitation than to changes in precipitation alone. Our results suggest that sensitivity to changes in climate cannot be predicted simply by knowing locations within the species’ climate envelope. Many climate processes did not affect population growth rates in the predicted direction based on range position. Processes such as species‐interactions, local adaptation, and interactions with the physical landscape likely affect the responses we observed. Our work highlights the need to measure demographic responses to changing climate.     

Global warming and the disruption of plant-pollinator interactions

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

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     

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.     

Identifying potential evolutionary consequences of climate-driven phenological shifts

Climate change is shifting the phenology of many species throughout the world. While the interspecific consequences of these phenological shifts have been well documented, the intraspecific shifts and their resultant evolutionary consequences remain relatively unexplored. Here, we present a conceptual framework and overview of how phenological shifts within species can drive evolutionary change. We suggest that because the impacts of climate change are likely to vary across the range of a species and differentially impact individuals, phenological shifts may often be highly variable both within and among populations. Together these changes have the potential to alter existing patterns of gene flow and influence evolutionary trajectories by increasing phenological isolation and connectivity. Recent research examining the response of species to contemporary climate change suggests that both phenological isolation and connectivity may be likely responses to future climate change. However, recent studies also show mixed results on whether adaptive responses to climate change are likely to occur, as some populations have already shown adaptive responses to changing climate, while others have not despite fitness costs. While predicting the exact consequences of intraspecific phenological shifts may be difficult, identifying the evolutionary implications of these shifts will allow a better understanding of the effects of future climate change on species persistence and adaptation.     

Food web de‐synchronization in England's largest lake: an assessment based on multiple phenological metrics

Phenological changes have been observed globally for marine, freshwater and terrestrial species, and are an important element of the global biological ‘fingerprint’ of climate change. Differences in rates of change could desynchronize seasonal species interactions within a food web, threatening ecosystem functioning. Quantification of this risk is hampered by the rarity of long‐term data for multiple interacting species from the same ecosystem and by the diversity of possible phenological metrics, which vary in their ecological relevance to food web interactions. We compare phenological change for phytoplankton (chlorophyll a), zooplankton (Daphnia) and fish (perch, Perca fluviatilis) in two basins of Windermere over 40 years and determine whether change has differed among trophic levels, while explicitly accounting for among‐metric differences in rates of change. Though rates of change differed markedly among the nine metrics used, seasonal events shifted earlier for all metrics and trophic levels: zooplankton advanced most, and fish least, rapidly. Evidence of altered synchrony was found in both lake basins, when combining information from all phenological metrics. However, comparisons based on single metrics did not consistently detect this signal. A multimetric approach showed that across trophic levels, earlier phenological events have been associated with increasing water temperature. However, for phytoplankton and zooplankton, phenological change was also associated with changes in resource availability. Lower silicate, and higher phosphorus, concentrations were associated with earlier phytoplankton growth, and earlier phytoplankton growth was associated with earlier zooplankton growth. The developing trophic mismatch detected between the dominant fish species in Windermere and important zooplankton food resources may ultimately affect fish survival and portend significant impacts upon ecosystem functioning. We advocate that future studies on phenological synchrony combine data from multiple phenological metrics, to increase confidence in assessments of change and likely ecological consequences.     

Community‐wide changes in intertaxonomic temporal co‐occurrence resulting from phenological shifts

Global climate change is known to affect the assembly of ecological communities by altering species' spatial distribution patterns, but little is known about how climate change may affect community assembly by changing species' temporal co‐occurrence patterns, which is highly likely given the widely observed phenological shifts associated with climate change. Here, we analyzed a 29‐year phenological data set comprising community‐level information on the timing and span of temporal occurrence in 11 seasonally occurring animal taxon groups from 329 local meteorological observatories across China. We show that widespread shifts in phenology have resulted in community‐wide changes in the temporal overlap between taxa that are dominated by extensions, and that these changes are largely due to taxa's altered span of temporal occurrence rather than the degree of synchrony in phenological shifts. Importantly, our findings also suggest that climate change may have led to less phenological mismatch than generally presumed, and that the context under which to discuss the ecological consequences of phenological shifts should be expanded beyond asynchronous shifts.     

Phenological asynchrony in plant–butterfly interactions associated with climate: a community‐wide perspective

Although much information has been accumulated on the effects of climate change on particular species worldwide, research aimed at assessing how such change influences biotic interactions from a community‐wide perspective is still in its infancy. We contribute to filling in this gap by analyzing a 17‐year (1996–2012) dataset that includes records of flower‐visitation interactions between 12 butterfly species and 17 plant species in a coastal wetland area in northeastern Iberian Peninsula. We assessed the extent to which temporal asynchronies between plants and adult butterflies are influenced by different climatic variables that affect both plant and insect phenologies. Temperature and degree of aridity at various monthly summaries were used as predictors of the plant–butterfly phenological asynchrony. We identified the seasonal window with the greatest effect on asynchronies for two butterfly generations (spring and summer), and assessed whether the magnitude of asynchrony is associated with the level of butterfly specialization. We used generalized linear mixed models considering a total of 39 plant–butterfly interactions. Average asynchrony was higher in the spring generation and dry conditions during winter lead to decreased temporal overlap with flowers in this butterfly generation, whereas dry conditions in the spring lead to decreased temporal overlap in the summer butterfly generation. The magnitude of the effect was consistently small at the community level (all interactions pooled). Moreover, no clear climatic trend over the study time frame was detected. Finally, specialized and generalized butterflies in their resource use as adults were similarly vulnerable to asynchronies, in contrast to previous predictions of greater mutualistic disruptions in species with narrower niches. We conclude that a least in the Mediterranean region, phenological asynchronies might be more affected by aridity level than by temperature itself, and thus the former can be a key climatic trait to make better predictions in this region.     

The eco‐evolutionary consequences of interspecific phenological asynchrony – a theoretical perspective

The timing of biological events (phenology) is an important aspect of both a species’ life cycle and how it interacts with other species and its environment. Patterns of phenological change have been given much scientific attention, particularly recently in relation to climate change. For pairs of interacting species, if their rates of phenological change differ, then this may lead to asynchrony between them and disruption of their ecological interactions. However it is often difficult to interpret differential rates of phenological change and to predict their ecological and evolutionary consequences. We review theoretical results regarding this topic, with special emphasis on those arising from life history theory, evolutionary game theory and population dynamic models. Much ecological research on phenological change builds upon the concept of match/mismatch, so we start by putting forward a simple but general model that captures essential elements of this concept. We then systematically compare the predictions of this baseline model with expectations from theory in which additional ecological mechanisms and features of species life cycles are taken into account. We discuss the ways in which the fitness consequences of interspecific phenological asynchrony may be weak, strong, or idiosyncratic. We discuss theory showing that synchrony is not necessarily an expected evolutionary outcome, and how population densities are not necessarily maximized by adaptation, and the implications of these findings. By bringing together theoretical developments regarding the eco‐evolutionary consequences of phenological asynchrony, we provide an overview of available alternative hypotheses for interpreting empirical patterns as well as the starting point for the next generation of theory in this field.     

Climate change has indirect effects on resource use and overlap among coexisting bird species with negative consequences for their reproductive success

Climate change can modify ecological interactions, but whether it can have cascading effects throughout ecological networks of multiple interacting species remains poorly studied. Climate‐driven alterations in the intensity of plant–herbivore interactions may have particularly profound effects on the larger community because plants provide habitat for a wide diversity of organisms. Here we show that changes in vegetation over the last 21 years, due to climate effects on plant–herbivore interactions, have consequences for songbird nest site overlap and breeding success. Browsing‐induced reductions in the availability of preferred nesting sites for two of three ground nesting songbirds led to increasing overlap in nest site characteristics among all three bird species with increasingly negative consequences for reproductive success over the long term. These results demonstrate that changes in the vegetation community from effects of climate change on plant–herbivore interactions can cause subtle shifts in ecological interactions that have critical demographic ramifications for other species in the larger community.     

Novel communities from climate change

Climate change is generating novel communities composed of new combinations of species. These result from different degrees of species adaptations to changing biotic and abiotic conditions, and from differential range shifts of species. To determine whether the responses of organisms are determined by particular species traits and how species interactions and community dynamics are likely to be disrupted is a challenge. Here, we focus on two key traits: body size and ecological specialization. We present theoretical expectations and empirical evidence on how climate change affects these traits within communities. We then explore how these traits predispose species to shift or expand their distribution ranges, and associated changes on community size structure, food web organization and dynamics. We identify three major broad changes: (i) Shift in the distribution of body sizes towards smaller sizes, (ii) dominance of generalized interactions and the loss of specialized interactions, and (iii) changes in the balance of strong and weak interaction strengths in the short term. We finally identify two major uncertainties: (i) whether large-bodied species tend to preferentially shift their ranges more than small-bodied ones, and (ii) how interaction strengths will change in the long term and in the case of newly interacting species.     

Limitations of population models in predicting climate change effects: a simulation study of sociable weavers in southern Africa

Current approaches for predicting climate change effects on populations comprise static models based on the geographical distribution of species, and dynamic population models based on the relationship between population processes and the recent variation in climate. Population models have the inherent advantage of considering a species’ response to climate as resulting from distinct mechanisms. However, they may have the disadvantage of considering only short‐term processes as they occur under the current climate, disregarding slowly adapting mechanisms. It would be important, however, to know whether slowly adapting processes occur, and whether they will respond to climate change. A way of testing for a discrepancy between short‐term and long‐term mechanisms in the response to climate is contrasting a population model with the current distribution and abundance in different climates. We demonstrate this idea for the sociable weaver Philetairussocius, a passerine bird of semiarid southern Africa. We develop a dynamic population model that predicts the species’ response to mean annual precipitation (MAP) and tests whether the model can reproduce the occurrence of sociable weavers in their current range of MAP as well as realistic abundances in two study locations with different MAP. The model predicts a decreased abundance under a scenario of decreased MAP and it can reproduce realistic populations in a single location. However it cannot explain the occurrence of sociable weavers across their entire distribution nor does it produce realistic abundances in the two areas when they were tested simultaneously. The results imply that the sensitive short‐term response to MAP is buffered by long‐term processes such as adaptation or plasticity in life history, shifts in interspecific interactions or changes in habitat structure. We suggest that this result is common for animals in semi‐arid and arid regions and discuss implications for static and dynamic modelling approaches in climate change research.     

Evolutionary relationships can be more important than abiotic conditions in predicting the outcome of plant–plant interactions

Positive and negative plant–plant interactions are major processes shaping plant communities. They are affected by environmental conditions and evolutionary relationships among the interacting plants. However, the generality of these factors as drivers of pairwise plant interactions and their combined effects remain virtually unknown. We conducted an observational study to assess how environmental conditions (altitude, temperature, irradiance and rainfall), the dispersal mechanism of beneficiary species and evolutionary relationships affected the co‐occurrence of pairwise interactions in 11 Stipa tenacissima steppes located along an environmental gradient in Spain. We studied 197 pairwise plant–plant interactions involving the two major nurse plants (the resprouting shrub Quercus coccifera and the tussock grass S. tenacissima) found in these communities. The relative importance of the studied factors varied with the nurse species considered. None of the factors studied were good predictors of the co‐ocurrence between S. tenacissima and its neighbours. However, both the dispersal mechanism of the beneficiary species and the phylogenetic distance between interacting species were crucial factors affecting the co‐occurrence between Q. coccifera and its neighbours, while climatic conditions (irradiance) played a secondary role. Values of phylogenetic distance between 207–272.8 Myr led to competition, while values outside this range or fleshy‐fruitness in the beneficiary species led to positive interactions. The low importance of environmental conditions as a general driver of pairwise interactions was caused by the species‐specific response to changes in either rainfall or radiation. This result suggests that factors other than climatic conditions must be included in theoretical models aimed to generally predict the outcome of plant–plant interactions. Our study helps to improve current theory on plant–plant interactions and to understand how these interactions can respond to expected modifications in species composition and climate associated to ongoing global environmental change.