Different currencies for calculating resource phenology result in opposite inferences about trophic mismatches.

Shifts in phenology are among the key responses of organisms to climate change. When rates of phenological change differ between interacting species they may result in phenological asynchrony. Studies have found conflicting patterns concerning the direction and magnitude of changes in synchrony, which have been attributed to biological factors. A hitherto overlooked additional explanation are differences in the currency used to quantify resource phenology, such as abundance and biomass. Studying an insectivorous bird (the sanderling) and its prey, we show that the median date of cumulative arthropod biomass occurred, on average, 6.9 days after the median date of cumulative arthropod abundance. In some years this difference could be as large as 21 days. For 23 years, hatch dates of sanderlings became less synchronized with the median date of arthropod abundance, but more synchronized with the median date of arthropod biomass. The currency-specific trends can be explained by our finding that mean biomass per arthropod specimen increased with date. Using a conceptual simulation, we show that estimated rates of phenological change for abundance and biomass can differ depending on temporal shifts in the size distribution of resources. We conclude that studies of trophic mismatch based on different currencies for resource phenology can be incompatible with each other.

Temperature has an overriding role compared to photoperiod in regulating the seasonal timing of winter moth egg hatching.

To accurately predict species' phenology under climate change, we need to gain a detailed mechanistic understanding of how different environmental cues interact to produce the seasonal timing response. In the winter moth (Operophtera brumata), seasonal timing of egg hatching is strongly affected by ambient temperature and has been under strong climate change-induced selection over the past 25 years. However, it is unclear whether photoperiod received at the egg stage also influences timing of egg hatching. Here, we investigated the relative contribution of photoperiod and temperature in regulating winter moth egg development using two split-brood experiments. We experimentally shifted the photoperiod eggs received by 2-4 weeks compared to the actual calendar date and measured the timing of egg hatching, both at a constant temperature and in combination with two naturally changing temperature treatments - mimicking a cold and a warm year. We found an eight-fold larger effect of temperature compared to photoperiod on egg development time. Moreover, the very small photoperiod effects we found were outweighed by both between- and within-clutch variation in egg development time. Thus, we conclude that photoperiod received at the egg stage does likely not play a substantial role in regulating the seasonal timing of egg hatching in the winter moth. These insights into the regulatory mechanism of seasonal timing could have important implications for predicting insect climate change adaptation, as we might expect different targets of selection depending on the relative contribution of different environmental cues.

Duration and variability of spring green-up mediate population consequences of climate change.

Single phenological measures, like the average rate of phenological advancement, may be insufficient to explain how climate change is driving trends in animal populations. Here, we develop a multifactorial concept of spring phenology-including the onset of spring, spring duration, interannual variability, and their temporal changes-as a driver for population dynamics of migratory terrestrial species in seasonal environments. Using this conceptual model, we found that effects of advancing spring phenology on animal populations may be buffered or amplified depending on the duration and interannual variability of spring green-up, and those effects are modified by evolutionary and plastic adaptations of species. Furthermore, we compared our modelling results with empirical data on normalized difference vegetation index-based spring green-up phenology and population trends of 106 European landbird finding similar associations. We conclude how phenological changes are expected to affect migratory bird populations across Europe and identify regions that are particularly prone to suffer population declines.

Feasting on the ordinary or starving for the exceptional in a warming climate: Phenological synchrony between spongy moth (Lymantria dispar) and budburst of six European tree species.

Global warming is affecting the phenological cycles of plants and animals, altering the complex synchronization that has co-evolved over thousands of years between interacting species and trophic levels. Here, we examined how warmer winter conditions affect the timing of budburst in six common European trees and the hatching of a generalist leaf-feeding insect, the spongy moth Lymantria dispar, whose fitness depends on the synchrony between egg hatch and leaf emergence of the host tree. We applied four different temperature treatments to L. dispar eggs and twig cuttings, that mimicked warmer winters and reduced chilling temperatures that are necessary for insect diapause and bud dormancy release, using heated open-top chambers (ambient or +3.5°C), and heated greenhouses (maintained at >6°C or >10°C). In addition, we conducted preference and performance tests to determine which tree species the larvae prefer and benefit from the most. Budburst success and twig survival were highest for all tree species at ambient temperature conditions, whereas it declined under elevated winter temperature for Tilia cordata and Acer pseudoplatanus, likely due to a lack of chilling. While L. dispar egg hatch coincided with budburst in most tree species within 10 days under ambient conditions, it coincided with budburst only in Quercus robur, Carpinus betulus, and, to a lesser extent, Ulmus glabra under warmer conditions. With further warming, we, therefore, expect an increasing mismatch in trees with high chilling requirements, such as Fagus sylvatica and A. pseudoplatanus, but still good synchronization with trees having low chilling requirements, such as Q. robur and C. betulus. Surprisingly, first instar larvae preferred and gained weight faster when fed with leaves of F. sylvatica, while Q. robur ranked second. Our results suggest that spongy moth outbreaks are likely to persist in oak and hornbeam forests in western and central Europe.

Climate change is associated with asynchrony in arrival between two sympatric cuckoos and both host arrival and prey emergence.

Matching the timing of spring arrival to the breeding grounds with hosts and prey is crucial for migratory brood parasites such as cuckoos. Previous studies have focused mostly on phenological mismatch between a single cuckoo species and its hosts but information regarding climate-driven mismatch between multiple sympatric cuckoo species and their hosts and invertebrate prey is still lacking. Here, we analysed long-term data (1988-2023) on the first arrival date of two declining migratory cuckoo species and their 14 migratory host species breeding in sympatry and prey emergence date in Tatarstan (southeast Russia). We found that the common cuckoo (Cuculus canorus; wintering in Africa) generally arrived on breeding grounds earlier than the oriental cuckoo (Cuculus optatus; wintering in southeast Asia and Australia). Both cuckoos have advanced their arrival dates over 36 years but less than their hosts, potentially resulting in an increasing arrival mismatch between cuckoos and their hosts. Moreover, cuckoo arrival advanced less than the emergence date of their prey over time. These observations indicate that climate change may disrupt co-fluctuation in the phenology of important life stages between multiple sympatric brood parasites, their hosts and prey with potential cascading consequences for population dynamics of involved species.

Phenological mismatch affects individual fitness and population growth in the winter moth.

Climate change can severely impact species that depend on temporary resources by inducing phenological mismatches between consumer and resource seasonal timing. In the winter moth, warmer winters caused eggs to hatch before their food source, young oak leaves, became available. This phenological mismatch changed the selection on the temperature sensitivity of egg development rate. However, we know little about the fine-scale fitness consequences of phenological mismatch at the individual level and how this mismatch affects population dynamics in the winter moth. To determine the fitness consequences of mistimed egg hatching relative to timing of oak budburst, we quantified survival and pupation weight in a feeding experiment. We found that mismatch greatly increased mortality rates of freshly hatched caterpillars, as well as affecting caterpillar growth and development time. We then investigated whether these individual fitness consequences have population-level impacts by estimating the effect of phenological mismatch on population dynamics, using our long-term data (1994-2021) on relative winter moth population densities at four locations in The Netherlands. We found a significant effect of mismatch on population density with higher population growth rates in years with a smaller phenological mismatch. Our results indicate that climate change-induced phenological mismatch can incur severe individual fitness consequences that can impact population density in the wild.

Effects of season of fire on bee-flower interaction diversity in a fire-maintained pine savanna.

Whereas the Coastal Plain of the southeastern United States historically experienced fire primarily during the mid-summer lightning season, managers today typically apply prescribed fire during the late winter or early spring months. The ecological implications of this discrepancy remain poorly understood, especially with regard to pollinators and their interactions with flowers. In a replicated field experiment, we compared the abundance and richness of bees and bee-flower interactions among pine savanna plots in Florida that were burned either during the winter, spring, summer, or fall. We netted 92 bee species from 77 species of flowers, representing 435 unique bee-flower interactions in total. When analyzing the results from each month separately, we detected significant short-term reductions in the number of bees and bee-flower interactions following fires regardless of season. Although bee abundance and richness did not differ over the entire season, bee-flower interaction richness was significantly higher overall in spring and summer plots than in fall plots and the composition of both bees and bee-flower interactions differed significantly among treatments. Several bee-flower interactions were significantly associated with one or more of the treatments. Some of these associations could be attributed to differences in flowering phenology among treatments. Taken together, our findings suggest that season of fire has modest but potentially important implications for interactions between bees and flowers in southeastern pine ecosystems. Because most flowering plants within our study region are pollinated by a variety of bees and other insects, and most bees endemic to the region are polylectic, season of fire may not be very important to either group overall. However, the timing of fire may be more important to particular species including certain flower specialists and fire-sensitive taxa such as butterflies. Future research targeting such species would be of interest.

Demographic consequences of phenological asynchrony for North American songbirds.

Changes in phenology in response to ongoing climate change have been observed in numerous taxa around the world. Differing rates of phenological shifts across trophic levels have led to concerns that ecological interactions may become increasingly decoupled in time, with potential negative consequences for populations. Despite widespread evidence of phenological change and a broad body of supporting theory, large-scale multitaxa evidence for demographic consequences of phenological asynchrony remains elusive. Using data from a continental-scale bird-banding program, we assess the impact of phenological dynamics on avian breeding productivity in 41 species of migratory and resident North American birds breeding in and around forested areas. We find strong evidence for a phenological optimum where breeding productivity decreases in years with both particularly early or late phenology and when breeding occurs early or late relative to local vegetation phenology. Moreover, we demonstrate that landbird breeding phenology did not keep pace with shifts in the timing of vegetation green-up over a recent 18-y period, even though avian breeding phenology has tracked green-up with greater sensitivity than arrival for migratory species. Species whose breeding phenology more closely tracked green-up tend to migrate shorter distances (or are resident over the entire year) and breed earlier in the season. These results showcase the broadest-scale evidence yet of the demographic impacts of phenological change. Future climate change-associated phenological shifts will likely result in a decrease in breeding productivity for most species, given that bird breeding phenology is failing to keep pace with climate change.

Phenotypic variation in the molt characteristics of a seasonal coat color-changing species reveals limited resilience to climate change.

The snowshoe hare (Lepus americanus) possesses a broad suite of adaptations to winter, including a seasonal coat color molt. Recently, climate change has been implicated in the range contraction of snowshoe hares along the southern range boundary. With shortening snow season duration, snowshoe hares are experiencing increased camouflage mismatch with their environment reducing survival. Phenological variation of hare molt at regional scales could facilitate local adaptation in the face of climate change, but the level of variation, especially along the southern range boundary, is unknown. Using a network of trail cameras and historical museum specimens, we (1) developed contemporary and historical molt phenology curves in the Upper Great Lakes region, USA, (2) calculated molt rate and variability in and among populations, and (3) quantified the relationship of molt characteristics to environmental conditions for snowshoe hares across North America. We found that snowshoe hares across the region exhibited similar fall and spring molt phenologies, rates and variation. Yet, an insular island population of hares on Isle Royale National Park, MI, completed their molt a week earlier in the fall and initiated molt almost 2 weeks later in the spring as well as exhibited slower rates of molting in the fall season compared to the mainland. Over the last 100 years, snowshoe hares across the region have not shifted in fall molt timing; though contemporary spring molt appears to have advanced by 17 days (~ 4 days per decade) compared to historical molt phenology. Our research indicates that some variation in molt phenology exists for snowshoe hares in the Upper Great Lakes region, but whether this variation is enough to offset the consequences of climate change remains to be seen.

Does coat colour influence survival? A test in a cyclic population of snowshoe hares.

Some mammal species inhabiting high-latitude biomes have evolved a seasonal moulting pattern that improves camouflage via white coats in winter and brown coats in summer. In many high-latitude and high-altitude areas, the duration and depth of snow cover has been substantially reduced in the last five decades. This reduction in depth and duration of snow cover may create a mismatch between coat colour and colour of the background environment, and potentially reduce the survival rate of species that depend on crypsis. We used long-term (1977-2020) field data and capture-mark-recapture models to test the hypothesis that whiteness of the coat influences winter apparent survival in a cyclic population of snowshoe hares (Lepus americanus) at Kluane, Yukon, Canada. Whiteness of the snowshoe hare coat in autumn declined during this study, and snowshoe hares with a greater proportion of whiteness in their coats in autumn survived better during winter. However, whiteness of the coat in spring did not affect subsequent summer survival. These results are consistent with the hypothesis that the timing of coat colour change in autumn can reduce overwinter survival. Because declines in cyclic snowshoe hare populations are strongly affected by low winter survival, the timing of coat colour change may adversely affect snowshoe hare population dynamics as climate change continues.

Current and lagged climate affects phenology across diverse taxonomic groups.

The timing of life events (phenology) can be influenced by climate. Studies from around the world tell us that climate cues and species' responses can vary greatly. If variation in climate effects on phenology is strong within a single ecosystem, climate change could lead to ecological disruption, but detailed data from diverse taxa within a single ecosystem are rare. We collated first sighting and median activity within a high-elevation environment for plants, insects, birds, mammals and an amphibian across 45 years (1975-2020). We related 10 812 phenological events to climate data to determine the relative importance of climate effects on species' phenologies. We demonstrate significant variation in climate-phenology linkage across taxa in a single ecosystem. Both current and prior climate predicted changes in phenology. Taxa responded to some cues similarly, such as snowmelt date and spring temperatures; other cues affected phenology differently. For example, prior summer precipitation had no effect on most plants, delayed first activity of some insects, but advanced activity of the amphibian, some mammals, and birds. Comparing phenological responses of taxa at a single location, we find that important cues often differ among taxa, suggesting that changes to climate may disrupt synchrony of timing among taxa.

Coat color mismatch improves survival of a keystone boreal herbivore: Energetic advantages exceed lost camouflage.

Climate warming is causing asynchronies between animal phenology and environments. Mismatched traits, such as coat color change mismatched with snow, can decrease survival. However, coat change does not serve a singular adaptive benefit of camouflage, and alternate coat change functions may confer advantages that supersede mismatch costs. We found that mismatch reduced, rather than increased, autumn mortality risk of snowshoe hares in Yukon by 86.5% when mismatch occurred. We suggest that the increased coat insulation and lower metabolic rates of winter-acclimatized hares confer energetic advantages to white mismatched hares that reduce their mortality risk. We found that white mismatched hares forage 17-77 min less per day than matched brown hares between 0°C and -10°C, thus lowering their predation risk and increasing survival. We found no effect of mismatch on spring mortality risk, during which mismatch occurred at warmer temperatures, suggesting a potential temperature limit at which the costs of conspicuousness outweigh energetic benefits.

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.

Colour moult phenology and camouflage mismatch in polymorphic populations of Arctic foxes.

Species that seasonally moult from brown to white to match snowy backgrounds become conspicuous and experience increased predation risk as snow cover duration declines. Long-term adaptation to camouflage mismatch in a changing climate might occur through phenotypic plasticity in colour moult phenology and or evolutionary shifts in moult rate or timing. Also, adaptation may include evolutionary shifts towards winter brown phenotypes that forgo the winter white moult. Most studies of these processes have occurred in winter white populations, with little attention to polymorphic populations with sympatric winter brown and winter white morphs. Here, we used remote camera traps to record moult phenology and mismatch in two polymorphic populations of Arctic foxes in Sweden over 2 years. We found that the colder, more northern population moulted earlier in the autumn and later in the spring. Next, foxes moulted earlier in the autumn and later in the spring during colder and snowier years. Finally, white foxes experienced relatively low camouflage mismatch while blue foxes were mismatched against snowy backgrounds most of the autumn through the spring. Because the brown-on-white mismatch imposes no evident costs, we predict that as snow duration decreases, increasing blue morph frequencies might help facilitate species persistence.

Climate driven disruption of transitional alpine bumble bee communities.

Pollinators at high elevations face multiple threats from climate change including heat stress, failure to phenological match advancing flower resources and competitive pressure from range-expanding species of lower elevations. We conducted long-term multi-site surveys of alpine bumble bees to determine how phenology of range-stable and range-expanding species is responding to climate change. We ask whether bumble bee responses generate mismatches with floral resources, and whether these mismatches in turn promote community disruption and potential species replacement. In alpine environments of the central Rocky Mountains, range-stable and range-expanding bumble bees exhibit phenological mismatches with flowering host plants due to earlier flowering of preferred resources under warmer spring temperatures. However, workers of range-stable species are more canalised in their foraging schedules, exploiting a relatively narrow portion of the flowering season. Specifically, range-stable species show less variance in phenology in response to temporally and spatially changing conditions than range-expanding ones. Because flowering duration drives the seasonal abundance of floral resources at the landscape scale, we hypothesize that canalisation of phenology in alpine bumble bees could reduce their access to earlier or later season flowers. Warmer conditions are decreasing abundances of range-stable alpine bumble bees above the timberline, increasing abundance of range-expanding species, and facilitating a novel and more species-diverse bumble bee community. However, this trend is not explained by greater phenological mismatch of range-stable bees. Results suggest that conversion of historic habitats for cold-adapted alpine bumble bee species into refugia for more heat-tolerant congeners is disrupting bumble bee communities at high elevations, though the precise mechanisms accounting for these changes are not yet known. If warming continues, we predict that the transient increase in diversity due to colonization by historically low-elevation species will likely give way to declines of alpine bumble bees in the central Rocky Mountains.

The ecological implications of intra- and inter-species variation in phenological sensitivity.

Plant-pollinator mutualisms rely upon the synchrony of interacting taxa. Climate change can disrupt this synchrony as phenological responses to climate vary within and across species. However, intra- and interspecific variation in phenological responses is seldom considered simultaneously, limiting our understanding of climate change impacts on interactions among taxa across their ranges. We investigated how variation in phenological sensitivity to climate can alter ecological interactions simultaneously within and among species using natural history collections and citizen science data. We focus on a unique system, comprising a wide-ranged spring ephemeral with varying color morphs (Claytonia virginica) and its specialist bee pollinator (Andrena erigeniae). We found strongly opposing trends in the phenological sensitivities of plants vs their pollinators. Flowering phenology was more sensitive to temperature in warmer regions, whereas bee phenology was more responsive in colder regions. Phenological sensitivity varied across flower color morphs. Temporal synchrony between flowering and pollinator activity was predicted to change heterogeneously across the species' ranges in the future. Our work demonstrates the complexity and fragility of ecological interactions in time and the necessity of incorporating variation in phenological responses across multiple axes to understand how such interactions will change in the future.

Different factors limit early- and late-season windows of opportunity for monarch development.

Seasonal windows of opportunity are intervals within a year that provide improved prospects for growth, survival, or reproduction. However, few studies have sufficient temporal resolution to examine how multiple factors combine to constrain the seasonal timing and extent of developmental opportunities. Here, we document seasonal changes in milkweed (Asclepias fascicularis)-monarch (Danaus plexippus) interactions with high resolution throughout the last three breeding seasons prior to a precipitous single-year decline in the western monarch population. Our results show early- and late-season windows of opportunity for monarch recruitment that were constrained by different combinations of factors. Early-season windows of opportunity were characterized by high egg densities and low survival on a select subset of host plants, consistent with the hypothesis that early-spring migrant female monarchs select earlier-emerging plants to balance a seasonal trade-off between increasing host plant quantity and decreasing host plant quality. Late-season windows of opportunity were coincident with the initiation of host plant senescence, and caterpillar success was negatively correlated with heatwave exposure, consistent with the hypothesis that late-season windows were constrained by plant defense traits and thermal stress. Throughout this study, climatic and microclimatic variations played a foundational role in the timing and success of monarch developmental windows by affecting bottom-up, top-down, and abiotic limitations. More exposed microclimates were associated with higher developmental success during cooler conditions, and more shaded microclimates were associated with higher developmental success during warmer conditions, suggesting that habitat heterogeneity could buffer the effects of climatic variation. Together, these findings show an important dimension of seasonal change in milkweed-monarch interactions and illustrate how different biotic and abiotic factors can limit the developmental success of monarchs across the breeding season. These results also suggest the potential for seasonal sequences of favorable or unfavorable conditions across the breeding range to strongly affect monarch population dynamics.

Temporal skewness of pollination success in the spring ephemeral Trillium camschatcense.

Phenological overlap with pollinators is crucial for reproductive success in insect-pollinated plants. In this study, we examined whether pollinator visitation successfully occurred during an entire flowering season in two populations of the insect-pollinated spring ephemeral Trillium camschatcense in the Tokachi region of Hokkaido, northern Japan. We bagged flowers and excluded pollinator visitation during either the first or the last half of the entire flowering season to compare pollination success between the two periods. The two populations have experienced differing levels of climate warming in the last 60 years, which impacted pollinator visitation. In the population experiencing temperature rise more rapidly, fertilization rate and seed set decreased sharply when bagged during the first half period, indicating that pollinator visitation is skewed to the early part of the flowering season. The temporal skewness of pollination success would be an early warning signal of the impacts of climate warming on the reproductive success of T. camschatcense.

Dynamic sensitivity to resource availability influences population responses to mismatches in a shorebird.

Climate change has caused shifts in seasonally recurring biological events leading to the temporal decoupling of consumer-resource pairs, that is, phenological mismatching. Although mismatches often affect individual fitness, they do not invariably scale up to affect populations, making it difficult to assess the risk they pose. Individual variation may contribute to this inconsistency, with changes in resource availability and consumer needs leading mismatches to have different outcomes over time. Nevertheless, most models estimate a consumer's match from a single time point, potentially obscuring when mismatches matter to populations. We analyzed how the effects of mismatches varied over time by studying precocial Hudsonian godwit (Limosa haemastica) chicks and their invertebrate prey from 2009 to 2019. We developed individual- and population-level models to determine how age-specific variation affects the relationship between godwits and resource availability. We found that periods with abundant resources led to higher growth and survival of godwit chicks, but also that chick survival was increasingly related to the availability of larger prey as chicks aged. At the population level, estimates of mismatches using age-structured consumer demand explained more variation in annual godwit fledging rates than more commonly used alternatives. Our study suggests that modeling the effects of mismatches as the disrupted interaction between dynamic consumer needs and resource availability clarifies when mismatches matter to both individuals and populations.