Quo vadis amphibia? Global warming and breeding phenology in frogs,toads and salamanders

As the earth is getting warmer, many animals and plants have shifted their timing of breeding towards earlier dates. However, there is substantial variation between populations in phenological shifts that typically goes unexplained. Identification of the different location and species characteristics that drive such variable responses to global warming is crucial if we are to make predictions for how projected climate change scenarios will play out on local and global scales. Here we conducted a phylogenetically controlled meta‐analysis of breeding phenology across frogs, toads and salamanders to examine the extent of variation in amphibian breeding phenology in response to global climate change. We show that there is strong geographic variation in response to global climate change, with species at higher latitudes exhibiting a more pronounced shift to earlier breeding than those at lower latitudes. Our analyses suggest that this latitude effect is a result of both the increased temperature (but not precipitation) at higher latitudes as well as a greater responsiveness by northern populations of amphibians to this change in temperature. We suggest that these effects should reinforce any direct effect of increasing warming at higher latitudes on breeding phenology. In contrast, we found very little contribution from other location factors or species traits. There was no evidence for a phylogenetic signal on advancing breeding phenology or responsiveness to temperature, suggesting that the amphibians that have been studied to date respond similarly to global warming.     

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.     

Predicting insect phenology across space and time

Many species appear to be undergoing shifts in phenology, arising from climate change. To predict the direction and magnitude of future changes requires an understanding of how phenology depends on climatic variation. Species show large‐scale spatial variation in phenology (affected by differentiation among populations) as well as variation in phenology from year‐to‐year at the same site (affected predominantly by local plasticity). Teasing apart spatial and temporal variation in phenology should allow improved predictions of phenology under climate change. This study is the first to quantify large‐scale spatial and temporal variation in the entire emergence pattern of species, and to test the relationships found by predicting future data. We use data from up to 33 years of permanent transect records of butterflies in the United Kingdom to fit and test models for 15 butterfly species. We use generalized additive models to model spatial and temporal variation in the distribution of adult butterflies over the season, allowing us to capture changes in the timing of emergence peaks, relative sizes of peaks and/or number of peaks in a single analysis. We develop these models using data for 1973–2000, and then use them to predict phenologies from 2001 to 2006. For six of our study species, a model with only spatial variation in phenology is the best predictor of the future, implying that these species have limited plasticity. For the remaining nine species, the best predictions come from a model with both spatial and temporal variation in phenology; for four of these, growing degree‐days have similar effects over space and time, implying high levels of plasticity. The results show that statistical phenology models can be used to predict phenology shifts in a second time period, suggesting that it should be feasible to project phenologies under climate change scenarios, at least over modest time scales.     

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.     

Mismatch Between Birth Date and Vegetation Phenology Slows the Demography of Roe Deer

Marked impacts of climate change on biodiversity have frequently been demonstrated, including temperature-related shifts in phenology and life-history traits. One potential major impact of climate change is the modification of synchronization between the phenology of different trophic levels. High phenotypic plasticity in laying date has allowed many bird species to track the increasingly early springs resulting from recent environmental change, but although changes in the timing of reproduction have been well studied in birds, these questions have only recently been addressed in mammals. To track peak resource availability, large herbivores like roe deer, with a widespread distribution across Europe, should also modify their life-history schedule in response to changes in vegetation phenology over time. In this study, we analysed the influence of climate change on the timing of roe deer births and the consequences for population demography and individual fitness. Our study provides a rare quantification of the demographic costs associated with the failure of a species to modify its phenology in response to a changing world. Given these fitness costs, the lack of response of roe deer birth dates to match the increasingly earlier onset of spring is in stark contrast with the marked phenotypic responses to climate change reported in many other mammals. We suggest that the lack of phenotypic plasticity in birth timing in roe deer is linked to its inability to track environmental cues of variation in resource availability for the timing of parturition.     

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.     

Ecological and methodological drivers of species’ distribution and phenology responses to climate change

Climate change is shifting species’ distribution and phenology. Ecological traits, such as mobility or reproductive mode, explain variation in observed rates of shift for some taxa. However, estimates of relationships between traits and climate responses could be influenced by how responses are measured. We compiled a global data set of 651 published marine species’ responses to climate change, from 47 papers on distribution shifts and 32 papers on phenology change. We assessed the relative importance of two classes of predictors of the rate of change, ecological traits of the responding taxa and methodological approaches for quantifying biological responses. Methodological differences explained 22% of the variation in range shifts, more than the 7.8% of the variation explained by ecological traits. For phenology change, methodological approaches accounted for 4% of the variation in measurements, whereas 8% of the variation was explained by ecological traits. Our ability to predict responses from traits was hindered by poor representation of species from the tropics, where temperature isotherms are moving most rapidly. Thus, the mean rate of distribution change may be underestimated by this and other global syntheses. Our analyses indicate that methodological approaches should be explicitly considered when designing, analysing and comparing results among studies. To improve climate impact studies, we recommend that (1) reanalyses of existing time series state how the existing data sets may limit the inferences about possible climate responses; (2) qualitative comparisons of species’ responses across different studies be limited to studies with similar methodological approaches; (3) meta‐analyses of climate responses include methodological attributes as covariates; and (4) that new time series be designed to include the detection of early warnings of change or ecologically relevant change. Greater consideration of methodological attributes will improve the accuracy of analyses that seek to quantify the role of climate change in species’ distribution and phenology changes.     

Phenological plasticity is a poor predictor of subalpine plant population performance following experimental climate change

Phenological shifts, changes in the seasonal timing of life cycle events, are among the best documented responses of species to climate change. However, the consequences of these phenological shifts for population dynamics remain unclear. Population growth could be enhanced if species that advance their phenology benefit from longer growing seasons and gain a pre-emptive advantage in resource competition. However, it might also be reduced if phenological advances increase exposure to stresses, such as herbivores and, in colder climates, harsh abiotic conditions early in the growing season. We exposed subalpine grasslands to ~3 K of warming by transplanting intact turfs from 2000 m to 1400 m elevation in the eastern Swiss Alps, with turfs transplanted within the 2000 m site acting as a control. In the first growing season after transplantation, we recorded species’ flowering phenology at both elevations. We also measured species’ cover change for three consecutive years as a measure of plant performance. We used models to estimate species’ phenological plasticity (the response of flowering time to the change in climate) and analysed its relationship with cover changes following climate change. The phenological plasticity of the 18 species in our study varied widely but was unrelated to their changes in cover. Moreover, early- and late-flowering species did not differ in their cover response to warming, nor in the relationship between cover changes and phenological plasticity. These results were replicated in a similar transplant experiment within the same subalpine community, established one year earlier and using larger turfs. We discuss the various ecological processes that can be affected by phenological shifts, and argue why the population-level consequences of these shifts are likely to be species- and context-specific. Our results highlight the importance of testing assumptions about how warming-induced changes in phenotypic traits, like phenology, impact population dynamics.     

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     

Climate variability and the timing of spring raptor migration in eastern North America

Many birds have advanced their spring migration and breeding phenology in response to climate change, yet some long‐distance migrants appear constrained in their adjustments. In addition, bird species with long generation times and those in higher trophic positions may also be less able to track climate‐induced shifts in food availability. Migratory birds of prey may therefore be particularly vulnerable to climate change because: 1) most are long‐lived and have relatively low reproductive capacity, 2) many feed predominately on insectivorous passerines, and 3) several undertake annual migrations totaling tens of thousands of kilometers. Using multi‐decadal datasets for 14 raptor species observed at six sites across the Great Lakes region of North America, we detected phenological shifts in spring migration consistent with decadal climatic oscillations and global climate change. While the North Atlantic and El Niño Southern Oscillations exerted heterogeneous effects on the phenology of a few species, arrival dates more generally advanced by 1.18 d per decade, a pattern consistent with the effects of global climate change. After accounting for heterogeneity across observation sites, five of the 10 most abundant species advanced the bulk of their spring migration phenology. Contrary to expectations, we found that long‐distance migrants and birds with longer generation times tended to make the greatest advancements to their spring migration. Such results may indicate that phenotypic plasticity can facilitate climatic responses among these long‐lived predators.     

Terrestrial insects and climate change: adaptive responses in key traits

Understanding and predicting how adaptation will contribute to species' resilience to climate change will be paramount to successfully managing biodiversity for conservation, agriculture, and human health‐related purposes. Making predictions that capture how species will respond to climate change requires an understanding of how key traits and environmental drivers interact to shape fitness in a changing world. Current trait‐based models suggest that low‐ to mid‐latitude populations will be most at risk, although these models focus on upper thermal limits, which may not be the most important trait driving species' distributions and fitness under climate change. In this review, we discuss how different traits (stress, fitness and phenology) might contribute and interact to shape insect responses to climate change. We examine the potential for adaptive genetic and plastic responses in these key traits and show that, although there is evidence of range shifts and trait changes, explicit consideration of what underpins these changes, be that genetic or plastic responses, is largely missing. Despite little empirical evidence for adaptive shifts, incorporating adaptation into models of climate change resilience is essential for predicting how species will respond under climate change. We are making some headway, although more data are needed, especially from taxonomic groups outside of Drosophila, and across diverse geographical regions. Climate change responses are likely to be complex, and such complexity will be difficult to capture in laboratory experiments. Moving towards well designed field experiments would allow us to not only capture this complexity, but also study more diverse species.     

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.     

Scale-dependent climate signals drive breeding phenology of three seabird species

Breeding at the right time is essential for animals in seasonal climates in order to ensure that the energy demands of reproduction, particularly the nutritional requirements of growing young, coincide with peak food availability. Global climate change is likely to cause shifts in the timing of peak food availability, and in order to adapt successfully to current and future climate change, animals need to be able to adjust the time at which they initiate breeding. Many animals use environmental cues available before the breeding season to predict the seasonal peak in food availability and adjust their phenology accordingly. We tested the hypothesis that regulation of breeding onset should reflect the scale at which organisms perceive their environment by comparing phenology of three seabird species at a North Sea colony. As predicted, the phenology of two dispersive species, black-legged kittiwake ( Rissa tridactyla ) and common guillemot ( Uria aalge ), correlated with a large-scale environmental cue (the North Atlantic Oscillation), whereas a resident species, European shag ( Phalacrocorax aristotelis ), was more affected by local conditions (sea surface temperature) around the colony. Annual mean breeding success was lower in late years for European shags, but not for the other two species. Since correlations among climate patterns at different scales are likely to change in the future, these findings have important implications for how migratory animals can respond to future climate change.     

Macrophenology: insights into the broad-scale patterns,drivers, and consequences of phenology

Plant phenology research has surged in recent decades, in part due to interest in phenological sensitivity to climate change and the vital role phenology plays in ecology. Many local-scale studies have generated important findings regarding the physiology, responses, and risks associated with shifts in plant phenology. By comparison, our understanding of regional- and global-scale phenology has been largely limited to remote sensing of green-up without the ability to differentiate among plant species. However, a new generation of analytical tools and data sources—including enhanced remote sensing products, digitized herbarium specimen data, and public participation in science—now permits investigating patterns and drivers of phenology across extensive taxonomic, temporal, and spatial scales, in an emerging field that we call macrophenology. Recent studies have highlighted how phenology affects dynamics at broad scales, including species interactions and ranges, carbon fluxes, and climate. At the cusp of this developing field of study, we review the theoretical and practical advances in four primary areas of plant macrophenology: (1) global patterns and shifts in plant phenology, (2) within-species changes in phenology as they mediate species' range limits and invasions at the regional scale, (3) broad-scale variation in phenology among species leading to ecological mismatches, and (4) interactions between phenology and global ecosystem processes. To stimulate future research, we describe opportunities for macrophenology to address grand challenges in each of these research areas, as well as recently available data sources that enhance and enable macrophenology research.     

Contrasting effects of warming and increased snowfall on Arctic tundra plant phenology over the past two decades

Recent changes in climate have led to significant shifts in phenology, with many studies demonstrating advanced phenology in response to warming temperatures. The rate of temperature change is especially high in the Arctic, but this is also where we have relatively little data on phenological changes and the processes driving these changes. In order to understand how Arctic plant species are likely to respond to future changes in climate, we monitored flowering phenology in response to both experimental and ambient warming for four widespread species in two habitat types over 21 years. We additionally used long‐term environmental records to disentangle the effects of temperature increase and changes in snowmelt date on phenological patterns. While flowering occurred earlier in response to experimental warming, plants in unmanipulated plots showed no change or a delay in flowering over the 21‐year period, despite more than 1 °C of ambient warming during that time. This counterintuitive result was likely due to significantly delayed snowmelt over the study period (0.05–0.2 days/yr) due to increased winter snowfall. The timing of snowmelt was a strong driver of flowering phenology for all species – especially for early‐flowering species – while spring temperature was significantly related to flowering time only for later‐flowering species. Despite significantly delayed flowering phenology, the timing of seed maturation showed no significant change over time, suggesting that warmer temperatures may promote more rapid seed development. The results of this study highlight the importance of understanding the specific environmental cues that drive species’ phenological responses as well as the complex interactions between temperature and precipitation when forecasting phenology over the coming decades. As demonstrated here, the effects of altered snowmelt patterns can counter the effects of warmer temperatures, even to the point of generating phenological responses opposite to those predicted by warming alone.     

Shifts in frog size and phenology: Testing predictions of climate change on a widespread anuran using data from prior to rapid climate warming

Changes in body size and breeding phenology have been identified as two major ecological consequences of climate change, yet it remains unclear whether climate acts directly or indirectly on these variables. To better understand the relationship between climate and ecological changes, it is necessary to determine environmental predictors of both size and phenology using data from prior to the onset of rapid climate warming, and then to examine spatially explicit changes in climate, size, and phenology, not just general spatial and temporal trends. We used 100 years of natural history collection data for the wood frog, Lithobates sylvaticus with a range >9 million km², and spatially explicit environmental data to determine the best predictors of size and phenology prior to rapid climate warming (1901–1960). We then tested how closely size and phenology changes predicted by those environmental variables reflected actual changes from 1961 to 2000. Size, phenology, and climate all changed as expected (smaller, earlier, and warmer, respectively) at broad spatial scales across the entire study range. However, while spatially explicit changes in climate variables accurately predicted changes in phenology, they did not accurately predict size changes during recent climate change (1961–2000), contrary to expectations from numerous recent studies. Our results suggest that changes in climate are directly linked to observed phenological shifts. However, the mechanisms driving observed body size changes are yet to be determined, given the less straightforward relationship between size and climate factors examined in this study. We recommend that caution be used in “space‐for‐time” studies where measures of a species’ traits at lower latitudes or elevations are considered representative of those under future projected climate conditions. Future studies should aim to determine mechanisms driving trends in phenology and body size, as well as the impact of climate on population density, which may influence body size.     

Climate- and resource-driven long-term changes in dormice populations negatively affect hole-nesting songbirds

Global climate change has been shown to cause variable shifts in phenology in a variety of animals and unexpected outcomes across food chains are to be found. Here we examined how rising annual spring temperatures affected the interactions between seed masting, cavity nesting birds and dormice using long-term data from Eastern Czech Republic. We have shown that climate change was associated with unequal shifts in the phenology of two cavity-breeding groups: dormice and birds. Rising spring temperatures have progressively advanced the termination of hibernation for the edible dormouse Glis glis , a common bird predator, leading to an increasing overlap in the use of nesting boxes between dormice and birds. In contrast, only the collared flycatcher Ficedula albicollis , of the four cavity-nesting bird species, advanced its breeding dates in response to rising temperatures. At the same time, favourable weather conditions, coupled with good seed masting years, have been associated with a substantial rise in dormice numbers. Concurrent with the increasing dormice abundance, the number of bird nests destroyed significantly increased in three out of four bird species. We showed that while there was a significant change in the date that the dormice emerged from hibernation during the course of the study, it did not significantly contribute to predation levels when controlling for their abundance and timing of breeding in birds. We found that the increasing dormice abundance was the main factor causing high brood losses in birds, while the timing of breeding in birds had a variable effect between bird species. This study illustrates how changes in climate might affect organisms at various trophic levels with often unexpected outcomes. Limited evidence from other study organisms suggests that species most at risk are those at different trophic levels that do not shift at the same rate or in the same direction as their food resources, predators or competitors.     

Temperature alone does not explain phenological variation of diverse temperate plants under experimental warming

Anthropogenic climate change has altered temperate forest phenology, but how these trends will play out in the future is controversial. We measured the effect of experimental warming of 0.6–5.0 °C on the phenology of a diverse suite of 11 plant species in the deciduous forest understory (Duke Forest, North Carolina, USA) in a relatively warm year (2011) and a colder year (2013). Our primary goal was to dissect how temperature affects timing of spring budburst, flowering, and autumn leaf coloring for functional groups with different growth habits, phenological niches, and xylem anatomy. Warming advanced budburst of six deciduous woody species by 5–15 days and delayed leaf coloring by 18–21 days, resulting in an extension of the growing season by as much as 20–29 days. Spring temperature accumulation was strongly correlated with budburst date, but temperature alone cannot explain the diverse budburst responses observed among plant functional types. Ring‐porous trees showed a consistent temperature response pattern across years, suggesting these species are sensitive to photoperiod. Conversely, diffuse‐porous species responded differently between years, suggesting winter chilling may be more important in regulating budburst. Budburst of the ring‐porous Quercus alba responded nonlinearly to warming, suggesting evolutionary constraints may limit changes in phenology, and therefore productivity, in the future. Warming caused a divergence in flowering times among species in the forest community, resulting in a longer flowering season by 10‐16 days. Temperature was a good predictor of flowering for only four of the seven species studied here. Observations of interannual temperature variability overpredicted flowering responses in spring‐blooming species, relative to our warming experiment, and did not consistently predict even the direction of flowering shifts. Experiments that push temperatures beyond historic variation are indispensable for improving predictions of future changes in phenology.     

Temperature‐related shifts in butterfly phenology depend on the habitat

Many species are becoming active earlier in the season as the climate becomes warmer. In parallel to phenological responses to climate change, many species have also been affected by habitat changes due to anthropogenic land use. As habitat type can directly affect microclimatic conditions, concurrent changes in climate and habitat could have interacting effects on the phenology of species. Temperature‐related shifts in phenology, however, have mostly been studied independent of habitat types. Here, I used long‐term data from a highly standardized monitoring program with 519 transects to study how phenology of butterflies is affected by ambient temperature and habitat type. I compared forests, agricultural areas and settlements, reflecting three major land use forms, and considered butterfly species that were observed in all three of these habitats. Seasonal appearance of the butterflies was affected both by the ambient temperature and the habitat type. As expected, warmer temperatures led to an overall advancement of the appearance and flight period of most species. Surprisingly, however, phenology of species was delayed in settlement habitats, even though this habitat type is generally associated with higher temperatures. A possible explanation is dispersal among habitat types, such that source–sink effects affect local phenology. When there is little productivity in settlement areas, observed butterflies may have immigrated from forest or agricultural habitats and thus appear later in settlements. My findings suggest that a spillover of individuals among habitats may affect phenology trends and indicate that phenological studies need to be interpreted in the context of habitat types. This becomes especially important when defining strategies to prevent or mitigate effects of climate and land‐use changes on phenology and abundance of species.     

Stage‐dependent physiological responses in a butterfly cause non‐additive effects on phenology

Studies illustrating climate‐induced shifts in phenology typically focus on the timing of a single lifecycle stage. In contrast, species’ responses to climate change are likely to be complex and constrained by interactions and tradeoffs across the lifecycle. We characterized the thermal sensitivity of egg, larval and pupal stages of a native Australian butterfly and then integrated these responses to predict sensitivity of emergence time, survival, and feeding performance on oviposition date and climate. Thermal physiology varied among lifecycle stages and between sexes, with the development rate of eggs, first instar larvae, and pupae being the most sensitive to temperature. As lifecycle stages have different thermal physiologies, the environment experienced by a given stage depends in a complex way on the experience of previous stages. Our simulations indicate that oviposition date strongly influences time spent in each lifecycle‐stage, as well as performance. Under a high emissions climate warming scenario (CSIRO Mk 3.5 climate model, high emissions SRES marker scenario A1F1, and a moderate rate of global warming), we predict development times to decrease by 38 days by 2070. Our analysis illustrates how differences in thermal physiology across the lifecycle may result in non‐additive effects on phenology which, in turn, may constrain species’ responses to global warming. These results highlight the need to view shifts in phenology in the context of an organism's entire lifecycle.