Time is of the essence: A general framework for uncovering temporal structures of communities.

Ecological communities are inherently dynamic: species constantly turn over within years, months, weeks or even days. These temporal shifts in community composition determine essential aspects of species interactions and how energy, nutrients, information, diseases and perturbations 'flow' through systems. Yet, our understanding of community structure has relied heavily on static analyses not designed to capture critical features of this dynamic temporal dimension of communities. Here, we propose a conceptual and methodological framework for quantifying and analysing this temporal dimension. Conceptually, we split the temporal structure into two definitive features, sequence and duration, and review how they are linked to key concepts in ecology. We then outline how we can capture these definitive features using perspectives and tools from temporal graph theory. We demonstrate how we can easily integrate ongoing research on phenology into this framework and highlight what new opportunities arise from this approach to answer fundamental questions in community ecology. As climate change reshuffles ecological communities worldwide, quantifying the temporal organization of communities is imperative to resolve the fundamental processes that shape natural ecosystems and predict how these systems may change in the future.

Longer days, larger grays: carryover effects of photoperiod and temperature in gray treefrogs, Hyla versicolor.

Environmental conditions like temperature and photoperiod can strongly shape organisms' growth and development. For many ectotherms with complex life cycles, global change will cause their offspring to experience warmer conditions and earlier-season photoperiods, two variables that can induce conflicting responses. We experimentally manipulated photoperiod and temperature during gray treefrog (Hyla versicolor) larval development to examine effects at metamorphosis and during short (10-day) and long (56-day) periods post-metamorphosis. Both early- and late-season photoperiods (April and August) decreased age and size at metamorphosis relative to the average-season (June) photoperiod, while warmer temperatures decreased age but increased size at metamorphosis. Warmer larval temperatures reduced short-term juvenile growth but had no long-term effect. Conversely, photoperiod had no short-term carryover effect, but juveniles from early- and late-season larval photoperiods had lower long-term growth rates than juveniles from the average-season photoperiod. Similar responses to early- and late-season photoperiods may be due to reduced total daylight compared with average-season photoperiods. However, juveniles from late-season photoperiods selected cooler temperatures than early-season juveniles, suggesting that not all effects of photoperiod were due to total light exposure. Our results indicate that despite both temperature and photoperiod affecting metamorphosis, the long-term effects of photoperiod may be much stronger than those of temperature.

Multiscale stability of an intertidal kelp (Postelsia palmaeformis) near its northern range edge through a period of prolonged heatwaves.

BACKGROUND AND AIMS: Climate change, including gradual changes and extreme weather events, is driving widespread species losses and range shifts. These climatic changes are felt acutely in intertidal ecosystems, where many organisms live close to their thermal limits and experience the extremes of both marine and terrestrial environments. A recent series of multiyear heatwaves in the northeast Pacific Ocean might have impacted species even towards their cooler, northern range edges. Among them, the high intertidal kelp Postelsia palmaeformis has traits that could make it particularly vulnerable to climate change, but it is critically understudied. METHODS: In 2021 and 2022, we replicated in situ and aerial P. palmaeformis surveys that were conducted originally in 2006 and 2007, in order to assess the state of northern populations following recent heatwaves. Changes in P. palmaeformis distribution, extent, density and morphometrics were assessed between these two time points over three spatial scales, ranging from 250 m grid cells across the entire 167 km study region, to within grid cells and the individual patch. KEY RESULTS: We found evidence consistent with population stability at all three scales: P. palmaeformis remained present in all 250 m grid cells in the study region where it was previously found, and neither the extent within cells nor the patch density changed significantly between time points. However, there was evidence of slight distributional expansion, increased blade lengths and a shift to earlier reproductive timing. CONCLUSIONS: We suggest that apparent long-term stability of P. palmaeformis might be attributable to thermal buffering near its northern range edge and from the wave-exposed coastlines it inhabits, which may have decreased the impacts of heatwaves. Our results highlight the importance of multiscale assessments when examining changes within species and populations, in addition to the importance of dispersal capability and local conditions in regulating the responses of species to climate change.

Effects of phenological mismatch under warming are modified by community context.

Climate change is altering the relative timing of species interactions by shifting when species first appear in communities and modifying the duration organisms spend in each developmental stage. However, community contexts, such as intraspecific competition and alternative resource species, can prolong shortened windows of availability and may mitigate the effects of phenological shifts on species interactions. Using a combination of laboratory experiments and dynamic simulations, we quantified how the effects of phenological shifts in Drosophila-parasitoid interactions differed with concurrent changes in temperature, intraspecific competition, and the presence of alternative host species. Our study confirmed that warming shortens the window of host susceptibility. However, the presence of alternative host species sustained interaction persistence across a broader range of phenological shifts than pairwise interactions by increasing the degree of temporal overlap with suitable development stages between hosts and parasitoids. Irrespective of phenological shifts, parasitism rates declined under warming due to reduced parasitoid performance, which limited the ability of community context to manage temporally mismatched interactions. These results demonstrate that the ongoing decline in insect diversity may exacerbate the effects of phenological shifts in ecological communities under future global warming temperatures.

Plasticity in female timing may explain earlier breeding in a North American songbird.

Many species have shifted their breeding phenology in response to climate change. Identifying the magnitude of phenological shifts and whether climate-mediated selection drives these shifts is key for determining species' resilience to climate change. Birds are a strong model for studying phenological shifts due to numerous long-term research studies; however, generalities pertaining to drivers of phenological shifts will emerge only as we add study species that differ in life history and geography. We investigated 32 years of reproductive timing in a non-migratory population of dark-eyed juncos Junco hyemalis. We predicted that plasticity in reproductive timing would allow females to breed earlier in warmer springs. We also predicted that selection would favour earlier breeding and asked whether the temperatures throughout the breeding season would predict the strength of selection. To test these predictions, we examined temporal changes in the annual median date for reproductive onset (i.e. first egg date) and we used a sliding window analysis to identify spring temperatures driving these patterns. Next, we explored plasticity in reproductive timing and asked whether selection favoured earlier breeding. Lastly, we used a sliding window analysis to identify the time during the breeding season that temperature was most associated with selection favouring earlier breeding. First egg dates occurred earlier over time and strongly covaried with April temperatures. Furthermore, individual females that bred in at least 3 years typically bred earlier in warmer Aprils, exhibiting plastic responses to April temperature. We also found significant overall selection favouring earlier breeding (i.e. higher relative fitness with earlier first egg dates) and variation in selection for earlier breeding over time. However, temperature across diverse climatic windows did not predict the strength of selection. Our findings provide further evidence for the role of phenotypic plasticity in shifting phenology in response to earlier springs. We also provide evidence for the role of selection favouring earlier breeding, regardless of temperature, thus setting the stage for adaptive changes in female breeding phenology. We suggest for multi-brooded birds that advancing first egg dates likely increase the length of the breeding season, and therefore, reproductive success.

Estimating phenological sensitivity in contemporary vs. historical data sets: Effects of climate resolution and spatial scale.

PREMISE: Phenological sensitivity, or the degree to which a species' phenology shifts in response to warming, is an important parameter for comparing and predicting species' responses to climate change. Phenological sensitivity is often measured using herbarium specimens or local studies in natural populations. These approaches differ widely in spatiotemporal scales, yet few studies explicitly consider effects of the geographic extent and resolution of climate data when comparing phenological sensitivities quantified from different data sets for a given species. METHODS: We compared sensitivity of flowering phenology to growing degree days of the alpine plant Silene acaulis using two data sets: herbarium specimens and a 6 yr observational study in four populations at Niwot Ridge, Colorado, USA. We investigated differences in phenological sensitivity obtained using variable spatial scales and climate data sources. RESULTS: Herbarium specimens underestimated phenological sensitivity compared to observational data, even when herbarium samples were limited geographically or to nearby weather station data. However, when observational data were paired with broader-scale climate data, as is typically used in herbarium data sets, estimates of phenological sensitivity were more similar. CONCLUSIONS: This study highlights the potential for variation in data source, geographic scale, and accuracy of macroclimate data to produce very different estimates of phenological responses to climate change. Accurately predicting phenological shifts would benefit from comparisons between methods that estimate climate variables and phenological sensitivity over a variety of spatial scales.

Spring understory herbs flower later in intensively managed forests.

Many organisms respond to anthropogenic environmental change through shifts in their phenology. In plants, flowering is largely driven by temperature, and therefore affected by climate change. However, on smaller scales climatic conditions are also influenced by other factors, including habitat structure. A group of plants with a particularly distinct phenology are the understory herbs in temperate European forests. In these forests, management alters tree species composition (often replacing deciduous with coniferous species) and homogenizes stand structure, and as a consequence changes light conditions and microclimate. Forest management should thus also affect the phenology of understory herbs. To test this, we recorded the flowering phenology of 16 early-flowering herbs on 100 forest plots varying in management intensity, from near-natural to intensely managed forests, in central and southern Germany. We found that in forest stands with a high management intensity, such as Norway spruce plantations, the plants flowered on average about 2 weeks later than in unmanaged forests. This was largely because management also affected microclimate (e.g., spring temperatures of 5.9°C in managed coniferous, 6.7 in managed deciduous, and 7.0°C in unmanaged deciduous plots), which in turn affected phenology, with plants flowering later on colder and moister forest stands (+4.5 d per -1°C and 2.7 d per 10% humidity increase). Among forest characteristics, the percentage of conifers had the greatest influence on microclimate, but also the age, overall crown projection area, structural complexity and spatial distribution of the forest stands. Our study indicates that forest management alters plant phenology, with potential far-reaching consequences for the ecology and evolution of understorey communities. More generally, our study demonstrates that besides climate change other drivers of environmental change, too, can influence the phenology of organisms.

Region-specific phenological sensitivities and rates of climate warming generate divergent temporal shifts in flowering date across a species' range.

PREMISE: Forecasting how species will respond phenologically to future changes in climate is a major challenge. Many studies have focused on estimating species- and community-wide phenological sensitivities to climate to make such predictions, but sensitivities may vary within species, which could result in divergent phenological responses to climate change. METHODS: We used 743 herbarium specimens of the mountain jewelflower (Streptanthus tortuosus, Brassicaceae) collected over 112 years to investigate whether individuals sampled from relatively warm vs. cool regions differ in their sensitivity to climate and whether this difference has resulted in divergent phenological shifts in response to climate warming. RESULTS: During the past century, individuals sampled from warm regions exhibited a 20-day advancement in flowering date; individuals in cool regions showed no evidence of a shift. We evaluated two potential drivers of these divergent responses: differences between regions in (1) the degree of phenological sensitivity to climate and (2) the magnitude of climate change experienced by plants, or (3) both. Plants sampled from warm regions were more sensitive to temperature-related variables and were subjected to a greater degree of climate warming than those from cool regions; thus our results suggest that the greater temporal shift in flowering date in warm regions is driven by both of these factors. CONCLUSIONS: Our results are among the first to demonstrate that species exhibited intraspecific variation in sensitivity to climate and that this variation can contribute to divergent responses to climate change. Future studies attempting to forecast temporal shifts in phenology should consider intraspecific variation.

Predicting phenological shifts in a changing climate.

Phenological shifts constitute one of the clearest manifestations of climate warming. Advanced emergence is widely reported in high-latitude ectotherms, but a significant number of species exhibit delayed, or no change in, emergence. Here we present a mechanistic theoretical framework that reconciles these disparate observations and predicts population-level phenological patterns based solely on data on temperature responses of the underlying life history traits. Our model, parameterized with data from insects at different latitudes, shows that peak abundance occurs earlier in the year when warming increases the mean environmental temperature, but is delayed when warming increases the amplitude of seasonal fluctuations. We find that warming does not necessarily lead to a longer activity period in high-latitude species because it elevates summer temperatures above the upper limit for reproduction and development. Our findings both confirm and confound expectations for ectotherm species affected by climate warming: an increase in the mean temperature is more detrimental to low-latitude species adapted to high mean temperatures and low-amplitude seasonal fluctuations; an increase in seasonal fluctuations is more detrimental to high-latitude species adapted to low mean temperatures and high-amplitude fluctuations.

Resource limitation alters effects of phenological shifts on inter-specific competition.

Phenological shifts can alter the relative arrival time of competing species in natural communities, but predicting the consequences for species interactions and community dynamics is a major challenge. Here we show that differences in relative arrival time can lead to predictable priority effects that alter the outcome of competitive interactions. By experimentally manipulating the relative arrival time of two competing tadpole species across a resource gradient, we found that delaying relative arrival of a species reduced the interaction asymmetry between species and could even reverse competitive dominance. However, the strength of these priority effects was contingent on the abundance of the shared resource. Priority effects were generally weak when resources were limited, but increased at higher resource levels. Importantly, this context dependency could be explained by a shift in per capita interaction strength driven by a shift in relative body sizes of competitors. These results shed new light into the mechanisms that drive variation in priority effects and help predict consequences of phenological shifts across different environments.

Intra-annual plasticity of growth mediates drought resilience over multiple years in tropical seedling communities.

Precipitation patterns are changing across the globe causing more severe and frequent drought for many forest ecosystems. Although research has focused on the resistance of tree populations and communities to these novel precipitation regimes, resilience of forests is also contingent on recovery following drought, which remains poorly understood, especially in aseasonal tropical forests. We used rainfall exclusion shelters to manipulate the interannual frequency of drought for diverse seedling communities in a tropical forest and assessed resistance, recovery and resilience of seedling growth and mortality relative to everwet conditions. We found seedlings exposed to recurrent periods of drought altered their growth rates throughout the year relative to seedlings in everwet conditions. During drought periods, seedlings grew slower than seedlings in everwet conditions (i.e., resistance phase) while compensating with faster growth after drought (i.e., recovery phase). However, the response to frequent drought was species dependent as some species grew significantly slower with frequent drought relative to everwet conditions while others grew faster with frequent drought due to overcompensating growth during the recovery phase. In contrast, mortality was unrelated to rainfall conditions and instead correlated with differences in light. Intra-annual plasticity of growth and increased annual growth of some species led to an overall maintenance of growth rates of tropical seedling communities in response to more frequent drought. These results suggest these communities can potentially adapt to predicted climate change scenarios and that plasticity in the growth of species, and not solely changes in mortality rates among species, may contribute to shifts in community composition under drought.

Interactions between warming and soil moisture increase overlap in reproductive phenology among species in an alpine meadow.

Climate warming strongly influences reproductive phenology of plants in alpine and Arctic ecosystems. Here, we focus on phenological shifts caused by experimental warming in a typical alpine meadow on the Tibetan Plateau. Under soil water stress caused by warming, most plants in the alpine meadow advanced or delayed their reproductive events to be aligned with the timing of peak rainfall. As a result, warming significantly increased the temporal overlap among reproductive stages of early- and late-flowering species. In addition, we found that some species, for example the late-flowering species, were unable to produce flowers and fruits under warming with failed monsoon rains. The potentially warmer- and drier-growing seasons under climate change may similarly shift the phenological patterns and change species composition of these alpine systems.

Timing of a plant-herbivore interaction alters plant growth and reproduction.

Phenological shifts have the potential to change species interactions, but relatively few studies have used experimental manipulations to examine the effects of variation in timing of an interspecific interaction across a series of life stages of a species. Although previous experimental studies have examined the consequences of phenological timing in plant-herbivore interactions for both plants and their herbivores, less is known about their effects on subsequent plant reproduction. Here, we conducted an experiment to determine how shifts in the phenological timing of monarch (Danaus plexippus) larval herbivory affected milkweed (Asclepias fascicularis) host plant performance, including effects on growth and subsequent effects on flower and seed pod phenology and production. We found that variation in the timing of herbivory affected both plant growth and reproduction, with measurable effects several weeks to several months after herbivory ended. The timing of herbivory had qualitatively different effects on vegetative and reproductive biomass: early-season herbivory had the strongest effects on plant size, whereas late-season herbivory had the strongest effects on the production of viable seeds. These results show that phenological shifts in herbivory can have persistent and qualitatively different effects on different life stages across the season.

Dissecting impacts of phenological shifts for performance across biological scales.

Although phenological shifts in response to climate are often assumed to benefit species' performance and viability, phenology's role in allowing population persistence and mediating species-level responses in the face of climate change remain unclear. Here, we develop a framework to understand when and why phenological shifts at three biological scales will influence performance: individuals, populations, and macroecological patterns. Specifically, we highlight three underexplored assumptions: (i) individual variability in phenology does not affect population fitness; (ii) population growth rates are sensitive to vital rates affected by phenology; and (iii) phenology mediates species-level responses to climate change including patterns of extinction, invasion, and range shifts. We outline promising methods for understanding how phenological shifts will influence performance within and across biological scales.

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.

Shifts in phenological mean and synchrony interact to shape competitive outcomes.

Climate change-induced phenological shifts are ubiquitous and have the potential to disrupt natural communities by changing the timing of species interactions. Shifts in first and/or mean phenological date are well documented, but recent studies indicate that shifts in synchrony (individual variation around these metrics) can be just as common. However, we know little about how both types of phenological shifts interact to affect species interactions and communities. Here, we experimentally manipulated the hatching phenologies of two competing species of larval amphibians to address this conceptual gap. Specifically, we manipulated the relative mean hatching time (early, same, or late relative to competitor) and population synchrony (high, medium, or low levels of variation around the mean) in a full 3 × 3 factorial design to measure independent and interactive effects of phenological mean and population phenological synchrony on competitive outcomes. Our results indicate that phenological synchrony within a population strongly influences intraspecific competition by changing the density of individuals and relative strength of early- vs. late-arriving individuals. Individuals from high-synchrony populations competed symmetrically, whereas individuals from low-synchrony populations competed asymmetrically. At the community scale, shifts in population phenological synchrony interact with shifts in phenological mean to affect key demographic rates (survival, biomass export, per capita mass, and emergence timing) strongly. Furthermore, changes in mean timing of species interactions altered phenological synchrony within a population at the next life stage, and phenological synchrony at one life stage altered the mean timing of the next life stage. Thus, shifts in phenological synchrony within populations cannot only alter species interactions, but species interactions in turn can also drive shifts in phenology.

Complex spatiotemporal phenological shifts as a response to rainfall changes.

• Climatic warming produces significant gradual alterations in the timing of life-cycle events, and here we study the phenological effects of rainfall-pattern changes. • We conducted ecosystem field experiments that partially excluded rain and runoff during the growing season in a Mediterranean forest and in a mediterranean shrubland. Studies of time-series of leaf-unfolding, flowering and fruiting over the last 50 yr in central Catalonia were carried out, and greenup onset in the Iberian Peninsula was monitored by satellite images. • Experimental, historical and geographical changes in rainfall produced significant, complex and strongly species-specific, as well as spatially and temporally variable, phenological effects. Among these changes, it was found that in the Iberian Peninsula, greenup onset changes from spring (triggered by rising temperatures) in the northern cool-wet regions to autumn (triggered by the arrival of autumn rainfalls) in the southern warm-dry regions. Even in the mesic Mediterranean central Catalonia (NE of the peninsula) rainfall had a stronger relative influence than temperature on fruiting phenology. • The results show that changes in rainfall and water availability, an important driver of climate change, can cause complex phenological changes with likely far-reaching consequences for ecosystem and biosphere functioning and structure. The seasonal shift in the Iberian Peninsula further highlights this importance and indicates that vegetation may respond to climate change not only with gradual, but also with abrupt temporal and spatial, changes in the timing of greenup onset.

From medicine to butterflies and back again.

My research focuses on the current impacts of climate change on wildlife, from field-based work on butterflies to synthetic analyses of global impacts on a broad range of species across terrestrial and marine biomes. I work actively with governmental agencies and NGOs to help develop conservation assessment and planning tools aimed at preserving biodiversity in the face of climate change.