Similarities in butterfly emergence dates among populations suggest local adaptation to climate

Phenology shifts are the most widely cited examples of the biological impact of climate change, yet there are few assessments of potential effects on the fitness of individual organisms or the persistence of populations. Despite extensive evidence of climate‐driven advances in phenological events over recent decades, comparable patterns across species' geographic ranges have seldom been described. Even fewer studies have quantified concurrent spatial gradients and temporal trends between phenology and climate. Here we analyse a large data set (~129 000 phenology measures) over 37 years across the UK to provide the first phylogenetic comparative analysis of the relative roles of plasticity and local adaptation in generating spatial and temporal patterns in butterfly mean flight dates. Although populations of all species exhibit a plastic response to temperature, with adult emergence dates earlier in warmer years by an average of 6.4 days per °C, among‐population differences are significantly lower on average, at 4.3 days per °C. Emergence dates of most species are more synchronised over their geographic range than is predicted by their relationship between mean flight date and temperature over time, suggesting local adaptation. Biological traits of species only weakly explained the variation in differences between space‐temperature and time‐temperature phenological responses, suggesting that multiple mechanisms may operate to maintain local adaptation. As niche models assume constant relationships between occurrence and environmental conditions across a species' entire range, an important implication of the temperature‐mediated local adaptation detected here is that populations of insects are much more sensitive to future climate changes than current projections suggest.     

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.     

Linking warming effects on phenology,demography, and range expansion in a migratory bird population

Phenological changes in response to climate change have been recorded in many taxa, but the population‐level consequences of these changes are largely unknown. If phenological change influences demography, it may underpin the changes in range size and distribution that have been associated with climate change in many species. Over the last century, Icelandic black‐tailed godwits (Limosa limosa islandica) have increased 10‐fold in numbers, and their breeding range has expanded throughout lowland Iceland, but the environmental and demographic drivers of this expansion remain unknown. Here, we explore the potential for climate‐driven shifts in phenology to influence demography and range expansion. In warmer springs, Icelandic black‐tailed godwits lay their clutches earlier, resulting in advances in hatching dates in those years. Early hatching is beneficial as population‐wide tracking of marked individuals shows that chick recruitment to the adult population is greater for early hatched individuals. Throughout the last century, this population has expanded into progressively colder breeding areas in which hatch dates are later, but temperatures have increased throughout Iceland since the 1960s. Using these established relationships between temperature, hatching dates and recruitment, we show that these warming trends have the potential to have fueled substantial increases in recruitment throughout Iceland, and thus to have contributed to local population growth and expansion across the breeding range. The demographic consequences of temperature‐mediated phenological changes, such as the advances in lay dates and increased recruitment associated with early hatching reported here, may therefore be key processes in driving population size and range changes in response to climate change.     

Best environmental predictors of breeding phenology differ with elevation in a common woodland bird species

Temperatures in mountain areas are increasing at a higher rate than the Northern Hemisphere land average, but how fauna may respond, in particular in terms of phenology, remains poorly understood. The aim of this study was to assess how elevation could modify the relationships between climate variability (air temperature and snow melt‐out date), the timing of plant phenology and egg‐laying date of the coal tit (Periparus ater). We collected 9 years (2011–2019) of data on egg‐laying date, spring air temperature, snow melt‐out date, and larch budburst date at two elevations (~1,300 m and ~1,900 m asl) on a slope located in the Mont‐Blanc Massif in the French Alps. We found that at low elevation, larch budburst date had a direct influence on egg‐laying date, while at high‐altitude snow melt‐out date was the limiting factor. At both elevations, air temperature had a similar effect on egg‐laying date, but was a poorer predictor than larch budburst or snowmelt date. Our results shed light on proximate drivers of breeding phenology responses to interannual climate variability in mountain areas and suggest that factors directly influencing species phenology vary at different elevations. Predicting the future responses of species in a climate change context will require testing the transferability of models and accounting for nonstationary relationships between environmental predictors and the timing of phenological events.     

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

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

Climatic effects and phenological mismatch in cuckoo–host interactions: a role for host phenotypic plasticity in laying date?

Climatic effects on breeding phenology vary across organisms and therefore might promote a phenological mismatch in ecologically interacting species, including those engaged in coevolutionary interactions such as brood parasites and their hosts. Recent studies suggest that climatic induced changes in migration phenology may have mismatched cuckoos and their hosts in Europe. However, it is currently unknown whether cuckoo–host phenological mismatch results from different degrees of phenotypic plasticity or to different speeds of microevolutionary processes affecting hosts and parasites. Here we performed 1) cross‐sectional correlations between climate conditions and population level of phenological mismatch between the migratory brood parasite great spotted cuckoo Clamator glandarius and its main resident host in Europe, the magpie Pica pica; and 2) a longitudinal analysis to study within‐individual variation in breeding phenology for individual hosts experiencing different climate conditions over a period of nine years (2005–2013). Cross‐sectional analyses revealed independent and contrary effects of winter and spring temperature on magpie phenology: magpie hosts tend to breed earlier those years with lower February temperatures, however, high temperature in the first half of April spur individuals to lay eggs. Breeding phenology of cuckoos was tuned to that of their magpie host in time and duration. However, annual phenological mismatch between cuckoos and magpie hosts increased with NAO index and January temperature. Longitudinal analyses revealed high individual consistency in magpie host phenology, but a low influence of climate, suggesting that the climatic‐driven phenological mismatch between cuckoos and magpies at the population‐level cannot be explained by a host plastic response to climatic conditions.     

北京地区木本春季物候特征与生物学特性的关系

植物物候是植物生活史中的重要性状,也是指示气候与自然环境变化的重要指标,现已成为全球变化领域的研究热点之一。传统物候研究多假设物候由气候因素决定,如气温、降水、光照等,并主要从植物物候的年际变化角度探讨了气候因素对物候特征的影响。然而,不同物种的物候存在较大差异表明植物物候还与自身生物学特性（如系统发育和功能性状）有关,但植物生物学特性如何影响植物物候仍缺乏深入研究。基于北京地区44种木本植物1965-2018年的展叶始期和开花始期观测资料,以展叶始期和开花始期的3类物候特征（平均物候期、物候对温度的响应敏感度和物候期的积温需求）为例,探究植物物候特征与系统发育和功能性状的关系。首先,利用系统发育信号Blomberg’s K和进化模型检验植物物候特征是否具有系统发育保守性,并通过系统发育信号表征曲线直观表达植物物候特征的进化模式;之后,利用广义估计方程分析植物生活型、传粉型与物候特征的关系,以揭示不同植物的资源利用方式及生存策略的差异。研究发现：（1）除展叶始期的温度敏感度外,其余物候特征的进化均受随机遗传漂变和自然选择力的共同作用,可推断物候特征具有系统发育保守性,即亲缘关系越近的物种物候特征越相似。（2）开花始期的系统发育信号强度比展叶始期更大,表明繁殖物候的系统发育可能比生长物候更保守。（3）植物展叶始期及其积温需求与生活型密切相关。灌木比乔木的展叶时间早、积温需求少。植物开花始期与传粉型相关,风媒植物开花显著早于虫媒植物。研究成果有助于深入理解物候变化的生物学机制,对于丰富物候学的理论研究有重要意义,同时对植物保护也具有重要的指导价值。     

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.     

Long‐term changes in autumn migration dates at the Strait of Gibraltar reflect population trends of soaring birds

A growing body of work shows that climate change is the cause of a number of directional shifts in the spring phenology of migratory birds. However, changes in autumn phenology are well studied and their consistency across species, as well as their link with population trends, remains uncertain. We investigate changes in the autumn migration dates of 11 species of soaring birds over the Strait of Gibraltar over a 16‐year period. Using models corrected for phylogeny, we assessed whether ecological and morphological characteristics, as well as population trends, account for interspecific shifts in migration times. We recorded different phenological changes in different periods of the migration season and suggest that these differences are due to age‐dependent responses. The variable best predicting advances in migration dates was population trend: species that did not advance their autumn migration dates were those showing a decline in their European breeding populations. We repeated our tests on a dataset representing the migration date of soaring birds across the Pyrenees Mountains and found that population trends at this site also predicted phenological shifts. Our results suggest that flexibility in migratory strategy and population trends may be related, such that different adaptive capacity in migration timing may be more relevant than other ecological traits in determining the conservation status of migratory birds in Europe and perhaps other regions.     

Tracking ice phenology by migratory waterbirds: settling phenology and breeding success of species with divergent population trends

Dependence on climate‐driven environmental cues in the initiation of life cycle stages is a critical attribute when assessing vulnerability of species to climate change impacts. This study focused on spring ice phenology as a cue to the settling of migratory waterbirds, asking whether there is an asynchrony between ice phenology and settling phenology that could affect breeding success of six species with divergent population trends. In the 37 study lakes in southeastern Finland, the ice‐out date not only varied considerably between years, but became progressively earlier during the study period, 1991–2018. Settling phenology of all species tracked inter‐annual variation in ice phenology. However, the degree of asynchrony between ice phenology and settling phenology varied between species, allowing discrimination between early and late settlers. Considerable inter‐annual variation also occurred within species, but in only one species did the degree of asynchrony correlate with the ice‐out date: for the horned grebe Podiceps auritus an earlier ice‐out date meant greater asynchrony between settling phenology and ice phenology. The degree of asynchrony between settling phenology and ice phenology did not affect breeding success in any species. However, ice phenology per se affected breeding success of horned grebes: earlier ice‐out was associated with lower annual breeding success. Breeding numbers of horned grebe showed a long‐term decline. Results suggest that short‐distance migratory birds are able to respond to climate change‐driven phenological changes in their breeding environments, and that this ability may not depend on the relative timing of breeding.     

Predicting the sensitivity of butterfly phenology to temperature over the past century

Studies to date have documented substantial variation among species in the degree to which phenology responds to temperature and shifts over time, but we have a limited understanding of the causes of such variation. Here, we use a spatially and temporally extensive data set (ca. 48 000 observations from across Canada) to evaluate the utility of museum collection records in detecting broad‐scale phenology‐temperature relationships and to test for systematic differences in the sensitivity of phenology to temperature (days °C^?1) of Canadian butterfly species according to relevant ecological traits. We showed that the timing of flight season predictably responded to temperature both across space (variation in average temperature from site to site in Canada) and across time (variation from year to year within each individual site). This reveals that collection records, a vastly underexploited resource, can be applied to the quantification of broad‐scale relationships between species' phenology and temperature. The timing of the flight season of earlier fliers and less mobile species was more sensitive to temperature than later fliers and more mobile species, demonstrating that ecological traits can account for some of the interspecific variation in species' phenological sensitivity to temperature. Finally, we found that phenological sensitivity to temperature differed across time and space implying that both dimensions of temperature will be needed to translate species' phenological sensitivity to temperature into accurate predictions of species' future phenological shifts. Given the widespread temperature sensitivity of flight season timing, we can expect long‐term temporal shifts with increased warming [ca. 2.4 days °C^?1 (0.18 SE)] for many if not most butterfly species.     

Phenological shifts assist colonisation of a novel environment in a range‐expanding raptor

In a rapidly changing world understanding the capacity of populations to adapt to novel environments is increasingly urgent. Timing of breeding can be a highly flexible trait and adjustments in this trait can potentially buffer populations from climate change and facilitate the colonisation of new environments. Recent range‐expansions into novel climatic regimes provide a valuable opportunity to investigate the implications of plasticity in timing of breeding for population processes. Black sparrowhawks have recently colonised the Cape Peninsula of South Africa where they experience dramatically different weather patterns to those in their historical range. These include a total reversal in the rainfall regime, with the majority of rain falling in the winter as opposed to the summer months. We investigate the breeding phenology of black sparrowhawks in relation to both regional and local climate variation and, using a long‐term dataset, explore the implications of phenological shifts for reproductive success and population growth following colonisation. In the recently colonised Cape Peninsula the breeding season began up to three months earlier than within their historical range and these early breeding attempts produced more offspring. Population models suggested that this adjustment assisted the colonisation of the Cape Peninsula, reducing the probability of extinction by 23%. Contrary to expectations, we found little support for the hypothesis that black sparrowhawks were responding to local variation in rainfall. We suggest that shifts in breeding phenology may be driven in part by other novel processes, such as interspecific competition for nest sites and lower temperatures during late summer. These results provide insight into the processes that facilitated the colonisation of a novel climatic regime highlighting the potential role of a diverse range of factors.     

Changes in satellite‐derived spring vegetation green‐up date and its linkage to climate in China from 1982 to 2010: a multimethod analysis

The change in spring phenology is recognized to exert a major influence on carbon balance dynamics in temperate ecosystems. Over the past several decades, several studies focused on shifts in spring phenology; however, large uncertainties still exist, and one understudied source could be the method implemented in retrieving satellite‐derived spring phenology. To account for this potential uncertainty, we conducted a multimethod investigation to quantify changes in vegetation green‐up date from 1982 to 2010 over temperate China, and to characterize climatic controls on spring phenology. Over temperate China, the five methods estimated that the vegetation green‐up onset date advanced, on average, at a rate of 1.3 ± 0.6 days per decade (ranging from 0.4 to 1.9 days per decade) over the last 29 years. Moreover, the sign of the trends in vegetation green‐up date derived from the five methods were broadly consistent spatially and for different vegetation types, but with large differences in the magnitude of the trend. The large intermethod variance was notably observed in arid and semiarid vegetation types. Our results also showed that change in vegetation green‐up date is more closely correlated with temperature than with precipitation. However, the temperature sensitivity of spring vegetation green‐up date became higher as precipitation increased, implying that precipitation is an important regulator of the response of vegetation spring phenology to change in temperature. This intricate linkage between spring phenology and precipitation must be taken into account in current phenological models which are mostly driven by temperature.     

Climate change,phenological shifts,eco-evolutionary responses and population viability: toward a unifying predictive approach

The debate on emission targets of greenhouse gasses designed to limit global climate change has to take into account the ecological consequences. One of the clearest ecological consequences is shifts in phenology. Linking these shifts to changes in population viability under various greenhouse gasses emission scenarios requires a unifying framework. We propose a box-in-a-box modeling approach that couples population models to phenological change. This approach unifies population modeling with both ecological responses to climate change as well as evolutionary processes. We advocate a mechanistic embedded correlative approach, where the link from genes to population is established using a periodic matrix population model. This periodic model has several major advantages: (1) it can include complex seasonal behaviors allowing an easy link with phenological shifts; (2) it provides the structure of the population at each phase, including the distribution of genotypes and phenotypes, allowing a link with evolutionary processes; and (3) it can incorporate the effect of climate at different time periods. We believe that the way climatologists have approached the problem, using atmosphere–ocean coupled circulation models in which components are gradually included and linked to each other, can provide a valuable example to ecologists. We hope that ecologists will take up this challenge and that our preliminary modeling framework will stimulate research toward a unifying predictive model of the ecological consequences of climate change.     

Warmer winters reduce frog fecundity and shift breeding phenology,which consequently alters larval development and metamorphic timing

One widely documented phenological response to climate change is the earlier occurrence of spring‐breeding events. While such climate change‐driven shifts in phenology are common, their consequences for individuals and populations have rarely been investigated. I addressed this gap in our knowledge by using a multi‐year observational study of six wood frog (Rana sylvatica) populations near the southern edge of their range. I tested first if winter temperature or precipitation affected the date of breeding and female fecundity, and second if timing of breeding affected subsequent larval development rate, mass at metamorphosis, date of metamorphosis, and survival. Warmer winters were associated with earlier breeding but reduced female fecundity. Winter precipitation did not affect breeding date, but was positively associated with female fecundity. There was no association between earlier breeding and larval survival or mass at metamorphosis, but earlier breeding was associated with delayed larval development. The delay in larval development was explained through a counterintuitive correlation between breeding date and temperature during larval development. Warmer winters led to earlier breeding, which in turn was associated with cooler post‐breeding temperatures that slowed larval development. The delay in larval development did not fully compensate for the earlier breeding, such that for every 2 days earlier that breeding took place, the average date of metamorphosis was 1 day earlier. Other studies have found that earlier metamorphosis is associated with increased postmetamorphic growth and survival, suggesting that earlier breeding has beneficial effects on wood frog populations.     

Arrival and onset of breeding of three passerine birds in eastern Finland tracks climatic variation and phenology of insects

Anthropogenic climate change poses a challenge to the annual cycles of migratory birds. It has become urgent to understand whether migratory birds are able to advance their spring phenology when the climate is warming and whether they are able to adjust these phenological phases to the spring phenology in their breeding areas. In this work, we studied long‐term trends in first arrival and onset of breeding for three passerine birds in eastern Finland; the pied flycatcher Ficedula hypoleuca, the common redstart Phoenicurus phoenicurus and the great tit Parus major. The pied flycatcher and the common redstart are long‐distance migrants while the great tit is a partial migrant in Finland. We asked what environmental variables best explain the first arrival or onset of breeding, if there is evidence of ‘thermal delay’ (long‐term increase in the accumulated temperatures) at arrival or onset of breeding and if the interannual variation in the onset of breeding correlates with variation in spring phenology of local insects. We found that the pied flycatcher and the common redstart had advanced their first arrival (explained by increased temperatures at the migration route), but we found no long‐term change in the onset of breeding (explained by local temperatures). Also, the onset of breeding of the great tit is tracking local temperatures. We found no or only weak evidence of thermal delay at arrival or onset of breeding for any of the species. The onsets of breeding for the pied flycatcher and the great tit are also closely tracking the spring phenology of the local insects. The stable or increasing population sizes of all three species in Finland could be a result from their ability to effectively track climatic and environmental variation.     

Phylogenetic conservatism and trait correlates of spring phenological responses to climate change in northeast China

Climate change has resulted in major changes in plant phenology across the globe that includes leaf‐out date and flowering time. The ability of species to respond to climate change, in part, depends on their response to climate as a phenological cue in general. Species that are not phenologically responsive may suffer in the face of continued climate change. Comparative studies of phenology have found phylogeny to be a reliable predictor of mean leaf‐out date and flowering time at both the local and global scales. This is less true for flowering time response (i.e., the correlation between phenological timing and climate factors), while no study to date has explored whether the response of leaf‐out date to climate factors exhibits phylogenetic signal. We used a 52‐year observational phenological dataset for 52 woody species from the Forest Botanical Garden of Heilongjiang Province, China, to test phylogenetic signal in leaf‐out date and flowering time, as well as, the response of these two phenological traits to both temperature and winter precipitation. Leaf‐out date and flowering time were significantly responsive to temperature for most species, advancing, on average, 3.11 and 2.87 day/°C, respectively. Both leaf‐out and flowering, and their responses to temperature exhibited significant phylogenetic signals. The response of leaf‐out date to precipitation exhibited no phylogenetic signal, while flowering time response to precipitation did. Native species tended to have a weaker flowering response to temperature than non‐native species. Earlier leaf‐out species tended to have a greater response to winter precipitation. This study is the first to assess phylogenetic signal of leaf‐out response to climate change, which suggests, that climate change has the potential to shape the plant communities, not only through flowering sensitivity, but also through leaf‐out sensitivity.     

Prairie plant phenology driven more by temperature than moisture in climate manipulations across a latitudinal gradient in the Pacific Northwest,USA

Plant phenology will likely shift with climate change, but how temperature and/or moisture regimes will control phenological responses is not well understood. This is particularly true in Mediterranean climate ecosystems where the warmest temperatures and greatest moisture availability are seasonally asynchronous. We examined plant phenological responses at both the population and community levels to four climate treatments (control, warming, drought, and warming plus additional precipitation) embedded within three prairies across a 520 km latitudinal Mediterranean climate gradient within the Pacific Northwest, USA. At the population level, we monitored flowering and abundances in spring 2017 of eight range‐restricted focal species planted both within and north of their current ranges. At the community level, we used normalized difference vegetation index (NDVI) measured from fall 2016 to summer 2018 to estimate peak live biomass, senescence, seasonal patterns, and growing season length. We found that warming exerted a stronger control than our moisture manipulations on phenology at both the population and community levels. Warming advanced flowering regardless of whether a species was within or beyond its current range. Importantly, many of our focal species had low abundances, particularly in the south, suggesting that establishment, in addition to phenological shifts, may be a strong constraint on their future viability. At the community level, warming advanced the date of peak biomass regardless of site or year. The date of senescence advanced regardless of year for the southern and central sites but only in 2018 for the northern site. Growing season length contracted due to warming at the southern and central sites (~3 weeks) but was unaffected at the northern site. Our results emphasize that future temperature changes may exert strong influence on the timing of a variety of plant phenological events, especially those events that occur when temperature is most limiting, even in seasonally water‐limited Mediterranean ecosystems.     

Advancing breeding phenology in response to environmental change in a wild red deer population

Most evidence for advances in phenology of in response to recent climate warming in wild vertebrate populations has come from long‐term studies of birds. Few studies have either documented phenological advances or tested their climatic causes and demographic consequences in wild mammal systems. Using a long‐term study of red deer on the Isle of Rum, Scotland, we present evidence of significant temporal trends in six phenological traits: oestrus date and parturition date in females, and antler cast date, antler clean date, rut start date and rut end date in males. These traits advanced by between 5 and 12 days across a 28‐year study period. Local climate measures associated with plant growth in spring and summer (growing degree days) increased significantly over time and explained a significant amount of variation in all six phenological traits, largely accounting for temporal advances observed in some of the traits. However, there was no evidence for temporal changes in key female reproductive performance traits (offspring birth weight and offspring survival) in this population, despite significant relationships between these traits and female phenology. In males, average antler weights increased over time presumably as a result of improved resource availability and physiological condition through spring and summer. There was no evidence for any temporal change in average male annual breeding success, as might be expected if the timing of male rutting behaviour was failing to track advances in the timing of oestrus in females. Our results provide rare evidence linking phenological advances to climate warming in a wild mammal and highlight the potential complexity of relationships between climate warming, phenology and demography in wild vertebrates.