Divergent trends in the risk of spring frost damage to trees in Europe with recent warming

Frost events during the active growth period of plants can cause extensive frost damage with tremendous economic losses and dramatic ecological consequences. A common assumption is that climate warming may bring along a reduction in the frequency and severity of frost damage to vegetation. On the other hand, it has been argued that rising temperature in late winter and early spring might trigger the so called “false spring”, that is, early onset of growth that is followed by cold spells, resulting in increased frost damage. By combining daily gridded climate data and 1,489 k in situ phenological observations of 27 tree species from 5,565 phenological observation sites in Europe, we show here that temporal changes in the risk of spring frost damage with recent warming vary largely depending on the species and geographical locations. Species whose phenology was especially sensitive to climate warming tended to have increased risk of frost damage. Geographically, compared with continental areas, maritime and coastal areas in Europe were more exposed to increasing occurrence of frost and these late spring frosts were getting more severe in the maritime and coastal areas. Our results suggest that even though temperatures will be elevated in the future, some phenologically responsive species and many populations of a given species will paradoxically experience more frost damage in the future warming climate. More attention should be paid to the increased frost damage in responsive species and populations in maritime areas when developing strategies to mitigate the potential negative impacts of climate change on ecosystems in the near future.     

Altered geographic and temporal variability in phenology in response to climate change

Aim In response to recent climate warming, numerous studies have reported an earlier onset of spring and, to a lesser degree, a later onset of autumn, both determined from phenological observations. Here, we examine whether these reported changes have affected the synchronization of events on a regional level by examining temporal and spatial variability in phenology. In particular, we study whether years with earlier springs are associated with an altered spatial variability in phenology. Location Germany and the United Kingdom. Methods Plant phenological observations of 35 different phases (events such as flowering and leafing) collected by the German Weather Service (1951–2002) and butterfly phenological records of 29 species collected by the UK Butterfly Monitoring Scheme (1976–2003) are used. In these long‐term records, we examine the temporal (year‐to‐year) variability and the spatial (geographic or between site) variability with particular emphasis on how they vary with time of the year and with earliness or lateness of the phase. Results Early phenological events (i.e. spring) are more variable than later events, both in time and in space, although the pattern is clearer for plants than for butterflies. Confirming previous results, we find a clear relationship between the mean date of spring and summer phases and the degree to which they have become earlier. The spatial variability of spring events is greater in warmer years that have faster plant development. However, late spring and summer events do not show a consistent relationship. Autumn events are somewhat more spatially variable in years characterized by later seasons. Main conclusions This is the first examination of spatial variability of plant and animal phenological events at a multinational scale. Earlier spring events are likely to be associated with increased spatial variability in plants, although this is unlikely to also be true for summer events. If species experience differential changes in geographic variation this may disrupt interactions among them, e.g. in food webs. On the other hand, these may offer advantages for mobile species. Further research on linked species is recommended.     

Impact of climate change on plant phenology in Mediterranean ecosystems

Plant phenology is strongly controlled by climate and has consequently become one of the most reliable bioindicators of ongoing climate change. We used a dataset of more than 200 000 records for six phenological events of 29 perennial plant species monitored from 1943 to 2003 for a comprehensive assessment of plant phenological responses to climate change in the Mediterranean region. Temperature, precipitation and North Atlantic Oscillation (NAO) were studied together during a complete annual cycle before phenological events to determine their relative importance and potential seasonal carry‐over effects. Warm and dry springs under a positive phase of NAO advance flowering, leaf unfolding and fruiting dates and lengthen the growing season. Spatial variability of dates (range among sites) was also reduced during warm and dry years, especially for spring events. Climate during previous weeks to phenophases occurrence had the greatest impact on plants, although all events were also affected by climate conditions several months before. Immediate along with delayed climate effects suggest dual triggers in plant phenology. Climatic models accounted for more than 80% of variability in flowering and leaf unfolding dates, and in length of the growing season, but for lower proportions in fruiting and leaf falling. Most part of year‐to‐year changes in dates was accounted for temperature, while precipitation and NAO accounted for <10% of dates' variability. In the case of flowering, insect‐pollinated species were better modelled by climate than wind‐pollinated species. Differences in temporal responses of plant phenology to recent climate change are due to differences in the sensitivity to climate among events and species. Spring events are changing more than autumn events as they are more sensitive to climate and are also undergoing the greatest alterations of climate relative to other seasons. In conclusion, climate change has shifted plant phenology in the Mediterranean region.     

Phenological change in a spring ephemeral: implications for pollination and plant reproduction

Climate change has had numerous ecological effects, including species range shifts and altered phenology. Altering flowering phenology often affects plant reproduction, but the mechanisms behind these changes are not well‐understood. To investigate why altering flowering phenology affects plant reproduction, we manipulated flowering phenology of the spring herb Claytonia lanceolata (Portulacaceae) using two methods: in 2011–2013 by altering snow pack (snow‐removal vs. control treatments), and in 2013 by inducing flowering in a greenhouse before placing plants in experimental outdoor arrays (early, control, and late treatments). We measured flowering phenology, pollinator visitation, plant reproduction (fruit and seed set), and pollen limitation. Flowering occurred approx. 10 days earlier in snow‐removal than control plots during all years of snow manipulation. Pollinator visitation patterns and strength of pollen limitation varied with snow treatments, and among years. Plants in the snow removal treatment were more likely to experience frost damage, and frost‐damaged plants suffered low reproduction despite lack of pollen limitation. Plants in the snow removal treatment that escaped frost damage had higher pollinator visitation rates and reproduction than controls. The results of the array experiment supported the results of the snow manipulations. Plants in the early and late treatments suffered very low reproduction due either to severe frost damage (early treatment) or low pollinator visitation (late treatment) relative to control plants. Thus, plants face tradeoffs with advanced flowering time. While early‐flowering plants can reap the benefits of enhanced pollination services, they do so at the cost of increased susceptibility to frost damage that can overwhelm any benefit of flowering early. In contrast, delayed flowering results in dramatic reductions in plant reproduction through reduced pollination. Our results suggest that climate change may constrain the success of early‐flowering plants not through plant‐pollinator mismatch but through the direct impacts of extreme environmental conditions.     

Cryptic phenology in plants: Case studies,implications, and recommendations

Plant phenology—the timing of cyclic or recurrent biological events in plants—offers insight into the ecology, evolution, and seasonality of plant‐mediated ecosystem processes. Traditionally studied phenologies are readily apparent, such as flowering events, germination timing, and season‐initiating budbreak. However, a broad range of phenologies that are fundamental to the ecology and evolution of plants, and to global biogeochemical cycles and climate change predictions, have been neglected because they are “cryptic”—that is, hidden from view (e.g., root production) or difficult to distinguish and interpret based on common measurements at typical scales of examination (e.g., leaf turnover in evergreen forests). We illustrate how capturing cryptic phenology can advance scientific understanding with two case studies: wood phenology in a deciduous forest of the northeastern USA and leaf phenology in tropical evergreen forests of Amazonia. Drawing on these case studies and other literature, we argue that conceptualizing and characterizing cryptic plant phenology is needed for understanding and accurate prediction at many scales from organisms to ecosystems. We recommend avenues of empirical and modeling research to accelerate discovery of cryptic phenological patterns, to understand their causes and consequences, and to represent these processes in terrestrial biosphere models.     

Experimental warming alters spring phenology of certain plant functional groups in an early successional forest community

Experimental study of the effects of projected climate change on plant phenology allows us to isolate effects of warming on life‐history events such as leaf out. We simulated a 2 °C temperature increase and 20% precipitation increase in a recently harvested temperate deciduous forest community in central Pennsylvania, USA, and observed the leaf out phenology of all species in 2009 and 2010. Over 130 plant species were monitored weekly in study plots, but due to high variability in species composition among plots, species were grouped into five functional groups: short forbs, tall forbs, shrubs, small trees, and large trees. Tall forbs and large trees, which usually emerge in the late spring, advanced leaf out 14–18 days in response to warming. Short forbs, shrubs, and small trees emerge early in spring and did not alter their phenology in response to warming or increased precipitation treatments. Earlier leaf out of tall forbs and large trees coincided with almost 3 weeks of increased community‐level leaf area index, indicating greater competition and a condensed spring green‐up period. While phenology of large trees and tall forbs appears to be strongly influenced by temperature‐based growth cues, our results suggest that photoperiod and chilling cues more strongly influence the leaf out of other functional groups. Reduced freeze events and warmer temperatures from predicted climate change will interact with nontemperature growth cues to have cascading consequences throughout the ecosystem.     

Temperature cues phenological synchrony in ant‐mediated seed dispersal

Species‐specific climate responses within ecological communities may disrupt the synchrony of co‐evolved mutualisms that are based on the shared timing of seasonal events, such as seed dispersal by ants (myrmecochory). The spring phenology of plants and ants coincides with marked changes in temperature, light and moisture. We investigate how these environmental drivers influence both seed release by early and late spring woodland herb species, and initiation of spring foraging by seed‐dispersing ants. We pair experimental herbaceous transplants with artificial ant bait stations across north‐ and south‐facing slopes at two contrasting geographic locations. This use of space enables robust identification of plant fruiting and ant foraging cues, and the use of transplants permits us to assess plasticity in plant phenology. We find that warming temperatures act as the primary phenological cue for plant fruiting and ant foraging. Moreover, the plasticity in plant response across locations, despite transplants being from the same source, suggests a high degree of portability in the seed‐dispersing mutualism. However, we also find evidence for potential climate‐driven facilitative failure that may lead to phenological asynchrony. Specifically, at the location where the early flowering species (Hepatica nobilis) is decreasing in abundance and distribution, we find far fewer seed‐dispersing ants foraging during its fruit set than during that of the later flowering Hexastylis arifolia. Notably, the key seed disperser, Aphaenogaster rudis, fails to emerge during early fruit set at this location. At the second location, A. picea forages equally during early and late seed release. These results indicate that climate‐driven changes might shift species‐specific interactions in a plant–ant mutualism resulting in winners and losers within the myrmecochorous plant guild.     

Phenological responses of plants to climate change in an urban environment

Global climate change is likely to alter the phenological patterns of plants due to the controlling effects of climate on plant ontogeny, especially in an urbanized environment. We studied relationships between various phenophases (i.e., seasonal biological events) and interannual variations of air temperature in three woody plant species (Prunus davidiana, Hibiscus syriacus, and Cercis chinensis) in the Beijing Metropolis, China, based on phenological data for the period 1962–2004 and meteorological data for the period 1951–2004. Analysis of phenology and climate data indicated significant changes in spring and autumn phenophases and temperatures. Changes in phenophases were observed for all the three species, consistent with patterns of rising air temperatures in the Beijing Metropolis. The changing phenology in the three plant species was reflected mainly as advances of the spring phenophases and delays in the autumn phenophases, but with strong variations among species and phenophases in response to different temperature indices. Most phenophases (both spring and autumn phenophases) had significant relationships with temperatures of the preceding months. There existed large inter- and intra-specific variations, however, in the responses of phenology to climate change. It is clear that the urban heat island effect from 1978 onwards is a dominant cause of the observed phenological changes. Differences in phenological responses to climate change may cause uncertain ecological consequences, with implications for ecosystem stability and function in urban environments.     

The influence of local spring temperature variance on temperature sensitivity of spring phenology

The impact of climate warming on the advancement of plant spring phenology has been heavily investigated over the last decade and there exists great variability among plants in their phenological sensitivity to temperature. However, few studies have explicitly linked phenological sensitivity to local climate variance. Here, we set out to test the hypothesis that the strength of phenological sensitivity declines with increased local spring temperature variance, by synthesizing results across ground observations. We assemble ground‐based long‐term (20–50 years) spring phenology database (PEP725 database) and the corresponding climate dataset. We find a prevalent decline in the strength of phenological sensitivity with increasing local spring temperature variance at the species level from ground observations. It suggests that plants might be less likely to track climatic warming at locations with larger local spring temperature variance. This might be related to the possibility that the frost risk could be higher in a larger local spring temperature variance and plants adapt to avoid this risk by relying more on other cues (e.g., high chill requirements, photoperiod) for spring phenology, thus suppressing phenological responses to spring warming. This study illuminates that local spring temperature variance is an understudied source in the study of phenological sensitivity and highlight the necessity of incorporating this factor to improve the predictability of plant responses to anthropogenic climate change in future studies.     

A reversal of the shift towards earlier spring phenology in several Mediterranean reptiles and amphibians during the 1998–2013 warming slowdown

Herps, especially amphibians, are particularly susceptible to climate change, as temperature tightly controls many parameters of their biological cycle—above all, their phenology. The timing of herps’ activity or migration period—in particular the dates of their first appearance in spring and first breeding—and the shift to earlier dates in response to warming since the last quarter of the 20^th century has often been described up to now as a nearly monotonic trend towards earlier phenological events. In this study, we used citizen science data opportunistically collected on reptiles and amphibians in the northern Mediterranean basin over a period of 32 years to explore temporal variations in herp phenology. For 17 common species, we measured shifts in the date of the species’ first spring appearance—which may be the result of current changes in climate—and regressed the first appearance date against temperatures and precipitations. Our results confirmed the expected overall trend towards earlier first spring appearances from 1983 to 1997, and show that the first appearance date of both reptiles and amphibians fits well with the temperature in late winter. However, the trend towards earlier dates was stopped or even reversed in most species between 1998 and 2013. We interpret this reversal as a response to cooling related to the North Atlantic Oscillation (NAO) in the late winter and early spring. During the positive NAO episodes, for certain species only (mainly amphibians), the effect of a warm weather, which tends to advance the phenology, seems to be counterbalanced by the adverse effects of the relative dryness.     

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

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

Testing a growth efficiency hypothesis with continental-scale phenological variations of common and cloned plants

Variation in the timing of plant phenology caused by phenotypic plasticity is a sensitive measure of how organisms respond to weather and climate variability. Although continental-scale gradients in climate and consequential patterns in plant phenology are well recognized, the contribution of underlying genotypic difference to the geography of phenology is less well understood. We hypothesize that different temperate plant genotypes require varying amount of heat energy for resuming annual growth and reproduction as a result of adaptation and other ecological and evolutionary processes along climatic gradients. In particular, at least for some species, the growing degree days (GDD) needed to trigger the same spring phenology events (e.g., budburst and flower bloom) may be less for individuals originated from colder climates than those from warmer climates. This variable intrinsic heat energy requirement in plants can be characterized by the term growth efficiency and is quantitatively reflected in the timing of phenophases—earlier timing indicates higher efficiency (i.e., less heat energy needed to trigger phenophase transitions) and vice versa compared to a standard reference (i.e., either a uniform climate or a uniform genotype). In this study, we tested our hypothesis by comparing variations of budburst and bloom timing of two widely documented plants from the USA National Phenology Network (i.e., red maple-Acer rubrum and forsythia-Forsythia spp.) with cloned indicator plants (lilac-Syringa x chinensis ‘Red Rothomagensis’) at multiple eastern US sites. Our results indicate that across the accumulated temperature gradient, the two non-clonal plants showed significantly more gradual changes than the cloned plants, manifested by earlier phenology in colder climates and later phenology in warmer climates relative to the baseline clone phenological response. This finding provides initial evidence supporting the growth efficiency hypothesis, and suggests more work is warranted. More studies investigating genotype-determined phenological variations will be useful for better understanding and prediction of the continental-scale patterns of biospheric responses to climate change.     

Phenological responses in a sycamore–aphid–parasitoid system and consequences for aphid population dynamics: A 20 year case study

Species interactions have a spatiotemporal component driven by environmental cues, which if altered by climate change can drive shifts in community dynamics. There is insufficient understanding of the precise time windows during which inter‐annual variation in weather drives phenological shifts and the consequences for mismatches between interacting species and resultant population dynamics—particularly for insects. We use a 20 year study on a tri‐trophic system: sycamore Acer pseudoplatanus, two associated aphid species Drepanosiphum platanoidis and Periphyllus testudinaceus and their hymenopteran parasitoids. Using a sliding window approach, we assess climatic drivers of phenology in all three trophic levels. We quantify the magnitude of resultant trophic mismatches between aphids and their plant hosts and parasitoids, and then model the impacts of these mismatches, direct weather effects and density dependence on local‐scale aphid population dynamics. Warmer temperatures in mid‐March to late‐April were associated with advanced sycamore budburst, parasitoid attack and (marginally) D. platanoidis emergence. The precise time window during which spring weather advances phenology varies considerably across each species. Crucially, warmer temperatures in late winter delayed the emergence of both aphid species. Seasonal variation in warming rates thus generates marked shifts in the relative timing of spring events across trophic levels and mismatches in the phenology of interacting species. Despite this, we found no evidence that aphid population growth rates were adversely impacted by the magnitude of mismatch with their host plants or parasitoids, or direct impacts of temperature and precipitation. Strong density dependence effects occurred in both aphid species and probably buffered populations, through density‐dependent compensation, from adverse impacts of the marked inter‐annual climatic variation that occurred during the study period. These findings explain the resilience of aphid populations to climate change and uncover a key mechanism, warmer winter temperatures delaying insect phenology, by which climate change drives asynchronous shifts between interacting species.     

Simulated climate warming alters phenological synchrony between an outbreak insect herbivore and host trees

As the world’s climate warms, the phenologies of interacting organisms in seasonally cold environments may advance at differing rates, leading to alterations in phenological synchrony that can have important ecological consequences. For temperate and boreal species, the timing of early spring development plays a key role in plant–herbivore interactions and can influence insect performance, outbreak dynamics, and plant damage. We used a field-based, meso-scale free-air forest warming experiment (B4WarmED) to examine the effects of elevated temperature on the phenology and performance of forest tent caterpillar (Malacosoma disstria) in relation to the phenology of two host trees, aspen (Populus tremuloides) and birch (Betula papyrifera). Results of our 2-year study demonstrated that spring phenology advanced for both insects and trees, with experimentally manipulated increases in temperature of 1.7 and 3.4 °C. However, tree phenology advanced more than insect phenology, resulting in altered phenological synchrony. Specifically, we observed a decrease in the time interval between herbivore egg hatch and budbreak of aspen in both years and birch in one year. Moreover, warming decreased larval development time from egg hatch to pupation, but did not affect pupal mass. Larvae developed more quickly on aspen than birch, but pupal mass was not affected by host species. Our study reveals that warming-induced phenological shifts can alter the timing of ecological interactions across trophic levels. These findings illustrate one mechanism by which climate warming could mediate insect herbivore outbreaks, and also highlights the importance of climate change effects on trophic interactions.     

Phenological Changes in the Southern Hemisphere

Current evidence of phenological responses to recent climate change is substantially biased towards northern hemisphere temperate regions. Given regional differences in climate change, shifts in phenology will not be uniform across the globe, and conclusions drawn from temperate systems in the northern hemisphere might not be applicable to other regions on the planet. We conduct the largest meta-analysis to date of phenological drivers and trends among southern hemisphere species, assessing 1208 long-term datasets from 89 studies on 347 species. Data were mostly from Australasia (Australia and New Zealand), South America and the Antarctic/subantarctic, and focused primarily on plants and birds. This meta-analysis shows an advance in the timing of spring events (with a strong Australian data bias), although substantial differences in trends were apparent among taxonomic groups and regions. When only statistically significant trends were considered, 82% of terrestrial datasets and 42% of marine datasets demonstrated an advance in phenology. Temperature was most frequently identified as the primary driver of phenological changes; however, in many studies it was the only climate variable considered. When precipitation was examined, it often played a key role but, in contrast with temperature, the direction of phenological shifts in response to precipitation variation was difficult to predict a priori. We discuss how phenological information can inform the adaptive capacity of species, their resilience, and constraints on autonomous adaptation. We also highlight serious weaknesses in past and current data collection and analyses at large regional scales (with very few studies in the tropics or from Africa) and dramatic taxonomic biases. If accurate predictions regarding the general effects of climate change on the biology of organisms are to be made, data collection policies focussing on targeting data-deficient regions and taxa need to be financially and logistically supported.     

Evidence of enhanced freezing damage in treeline plants during six years of CO2 enrichment and soil warming

Climate change and elevated atmospheric CO₂ levels could increase the vulnerability of plants to freezing. We analyzed tissue damage resulting from naturally occurring freezing events in plants from a long–term in situ CO₂ enrichment (+ 200 ppm, 2001–2009) and soil warming (+ 4°C since 2007) experiment at treeline in the Swiss Alps (Stillberg, Davos). Summer freezing events caused damage in several abundant subalpine and alpine plant species in four out of six years between 2005 and 2010. Most freezing damage occurred when temperatures dropped below –1.5°C two to three weeks after snow melt. The tree Larix decidua and the dwarf shrubs Vaccinium myrtillus and Empetrum hermaphroditum showed more freezing damage under experimentally elevated CO₂ and/or temperatures than under control conditions. Soil warming induced a 50% die‐back of E. hermaphroditum during a single freezing event due to melting of the protective snow cover. Although we could not identify a clear mechanism, we relate greater freezing susceptibility to a combination of advanced plant phenology in spring and changes in plant physiology. The climate record since 1975 at the treeline site indicated a summer warming by 0.58°C/decade and a 3.5 days/decade earlier snow melt, but no significant decrease in freezing events during the vegetation period. Therefore, in a warmer climate with higher CO₂ levels but constant likelihood of extreme weather events, subalpine and alpine plants may be more susceptible to freezing events, which may partially offset expected enhanced growth with global change. Hence, freezing damage should be considered when predicting changes in growth of alpine plants or changes in community composition under future atmospheric and climate conditions.     

Forecasting phenology under global warming

As a consequence of warming temperatures around the world, spring and autumn phenologies have been shifting, with corresponding changes in the length of the growing season. Our understanding of the spatial and interspecific variation of these changes, however, is limited. Not all species are responding similarly, and there is significant spatial variation in responses even within species. This spatial and interspecific variation complicates efforts to predict phenological responses to ongoing climate change, but must be incorporated in order to build reliable forecasts. Here, we use a long-term dataset (1953–2005) of plant phenological events in spring (flowering and leaf out) and autumn (leaf colouring and leaf fall) throughout Japan and South Korea to build forecasts that account for these sources of variability. Specifically, we used hierarchical models to incorporate the spatial variability in phenological responses to temperature to then forecast species'' overall and site-specific responses to global warming. We found that for most species, spring phenology is advancing and autumn phenology is getting later, with the timing of events changing more quickly in autumn compared with the spring. Temporal trends and phenological responses to temperature in East Asia contrasted with results from comparable studies in Europe, where spring events are changing more rapidly than are autumn events. Our results emphasize the need to study multiple species at many sites to understand and forecast regional changes in phenology.     

Phenology and climate change: a long-term study in a Mediterranean locality

It is well documented that plant and animal phenology is changing in response to recent climate warming in the Palaearctic. However, few long-term data sets are currently available in the Mediterranean basin. The present study reports long-term temporal trends of several phenophases of 45 plants, 4 insects and 6 migratory insectivorous birds. Dynamic factor analyses performed with plant phenophases showed that most of those events occurring at spring and summer had common trends toward the advancement, especially since mid-1970s. However, during these last decades, insect phenology showed a steeper advance than plant phenology, suggesting an increase of decoupling of some plant–insect interactions, such as those between pollinators and flowers or herbivorous insects and their plant resources. All trans-Saharan bird species showed highly significant temporal trends in all studied phenophases (some of them covering most of the last century). In two species, the duration of stay is increasing due to both earlier arrivals and later departures. On the other hand, two wintering species showed a significant advancement in their arrival dates, while an opposite pattern were found for departures of each one. Only one of these species increased significantly its wintering stay. Bird departures were not related to local climate in any species. Our results demonstrate a key role of local temperatures behind interannual variability of most plant and insects phenophases, with especial emphasis in those occurring in spring and summer. Therefore, the common signal towards the advancement recorded since mid-1970s resulted from the recent rise in temperatures.     

Climate warming,ecological mismatch at arrival and population decline in migratory birds

Climate is changing at a fast pace, causing widespread, profound consequences for living organisms. Failure to adjust the timing of life-cycle events to climate may jeopardize populations by causing ecological mismatches to the life cycle of other species and abiotic factors. Population declines of some migratory birds breeding in Europe have been suggested to depend on their inability to adjust migration phenology so as to keep track of advancement of spring events at their breeding grounds. In fact, several migrants have advanced their spring arrival date, but whether such advancement has been sufficient to compensate for temporal shift in spring phenophases or, conversely, birds have become ecologically mismatched, is still an unanswered question, with very few exceptions. We used a novel approach based on accumulated winter and spring temperatures (degree-days) as a proxy for timing of spring biological events to test if the progress of spring at arrival to the breeding areas by 117 European migratory bird species has changed over the past five decades. Migrants, and particularly those wintering in sub-Saharan Africa, now arrive at higher degree-days and may have therefore accumulated a ‘thermal delay’, thus possibly becoming increasingly mismatched to spring phenology. Species with greater ‘thermal delay’ have shown larger population decline, and this evidence was not confounded by concomitant ecological factors or by phylogenetic effects. These findings provide general support to the largely untested hypotheses that migratory birds are becoming ecologically mismatched and that failure to respond to climate change can have severe negative impacts on their populations. The novel approach we adopted can be extended to the analysis of ecological consequences of phenological response to climate change by other taxa.     

澳门九澳山海滨群落10种植物盛花期物候对极端气候事件的响应

为探究极端气候事件对植物的影响,对澳门九澳山海滨群落10种植物2012-2017年盛花期物候进行了观察。结果表明,植物的盛花期一般在3-9月,其中有4种植物为5月。2013和2016年早春澳门的极端强降水使植物的盛花期出现了明显的提前或者推迟。9种植物的盛花期与盛花期前0～2个月和上一年的秋冬季的月均温度或月降水存在显著相关性。温度和降水对植物盛花期的影响差异不大,但晚花植物对降水更加敏感。这为澳门和邻近岛屿的生态恢复和园林树种选材提供参考。