Effects of climatic change on the phenology of butterflies in the northwest Mediterranean Basin

Phenological changes in response to climatic warming have been detected across a wide range of organisms. Butterflies stand out as one of the most popular groups of indicators of climatic change, given that, firstly, they are poikilothermic and, secondly, have been the subject of thorough monitoring programmes in several countries for a number of decades. Here we provide for the first time strong evidence of phenological change as a consequence of recent climatic warming in butterflies at a Spanish site in the northwest Mediterranean Basin. By means of the widely used Butterfly Monitoring Scheme methodology, three different phenological parameters were analysed for the most common species to test for trends over time and relationships with temperature and precipitation. Between 1988 and 2002, there was a tendency for earlier first appearance dates in all 17 butterfly species tested, and significant advances in mean flight dates in 8 out of 19 species. On the other hand, the shape of the curve of adult emergence did not show any regular pattern. These changes paralleled an increase of 1–1.5°C in mean February, March and June temperatures. Likewise, a correlation analysis indicated the strong negative effect of spring temperature on phenological parameters (i.e. higher temperatures tended to produce phenological advances), and the opposite effect of precipitation in certain months. In addition, there was some evidence to indicate that phenological responses may differ between taxonomic lineages or species with similar diets. We discuss the consequences that these changes may have on species' population abundances, especially given the expected increase in aridity in the Mediterranean Basin caused by current climatic warming. We predict that varying degrees of phenological flexibility may account for differences in species' responses and, for multivoltine species, predict strong selection favouring local seasonal adaptations such as diapause phenomena or migratory behaviour.     

Spring predictability explains different leaf‐out strategies in the woody floras of North America,Europe and East Asia

Intuitively, interannual spring temperature variability (STV) should influence the leaf‐out strategies of temperate zone woody species, with high winter chilling requirements in species from regions where spring warming varies greatly among years. We tested this hypothesis using experiments in 215 species and leaf‐out monitoring in 1585 species from East Asia (EA), Europe (EU) and North America (NA). The results reveal that species from regions with high STV indeed have higher winter chilling requirements, and, when grown under the same conditions, leaf out later than related species from regions with lower STV. Since 1900, STV has been consistently higher in NA than in EU and EA, and under experimentally short winter conditions NA species required 84% more spring warming for bud break, EU ones 49% and EA ones only 1%. These previously unknown continental‐scale differences in phenological strategies underscore the need for considering regional climate histories in global change models.     

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.     

Shifting and extension of phenological periods with increasing temperature along elevational transects in southern Bavaria

The impact of global warming on phenology has been widely studied, and almost consistently advancing spring events have been reported. Especially in alpine regions, an extraordinary rapid warming has been observed in the last decades. However, little is known about phenological phases over the whole vegetation period at high elevations. We observed 12 phenological phases of seven tree species and measured air temperature at 42 sites along four transects of about 1000 m elevational range in the years 2010 and 2011 near Garmisch‐Partenkirchen, Germany. Site‐ and species‐specific onset dates for the phenological phases were determined and related to elevation, temperature lapse rates and site‐specific temperature sums. Increasing temperatures induced advanced spring and delayed autumn phases, in which both yielded similar magnitudes. Delayed leaf senescence could therefore have been underestimated until now in extending the vegetation period. Not only the vegetation period, but also phenological periods extended with increasing temperature. Moreover, sensitivity to elevation and temperature strongly depends on the specific phenological phase. Differences between species and groups of species (deciduous, evergreen, high elevation) were found in onset dates, phenological response rates and also in the effect of chilling and forcing temperatures. Increased chilling days highly reduced forcing temperature requirements for deciduous trees, but less for evergreen trees. The problem of shifted species associations and phenological mismatches due to species‐specific responses to increasing temperature is a recent topic in ecological research. Therefore, we consider our findings from this novel, dense observation network in an alpine area of particular importance to deepen knowledge on phenological responses to climate change.     

Climate controls on vegetation phenological patterns in northern mid- and high latitudes inferred from MODIS data

Recent studies using both field measurements and satellite-derived-vegetation indices have demonstrated that global warming is influencing vegetation growth and phenology. To accurately predict the future response of vegetation to climate variation, a thorough understanding of vegetation phenological cycles and their relationship to temperature and precipitation is required. In this paper, vegetation phenological transition dates identified using data from the moderate-resolution imaging spectroradiometer (MODIS) in 2001 are linked with MODIS land surface temperature (LST) data from the northern hemisphere between 35°N and 70°N. The results show well-defined patterns dependent on latitude, in which vegetation greenup gradually migrates northward starting in March, and dormancy spreads southward from late September. Among natural vegetation land-cover types, the growing-season length for forests is strongly correlated with variation in mean annual LST. For urban areas, the onset of greenup is 4–9 days earlier on average, and the onset of dormancy is about 2–16 days later, relative to adjacent natural vegetation. This difference (especially for urban vs. forests) is apparently related to urban heat island effects that result in both the average spring temperature and the mean annual temperature in urban areas being about 1–3°C higher relative to rural areas. The results also indicate that urban heat island effects on vegetation phenology are stronger in North America than in Europe and Asia. Finally, the onset of forest greenup at continental scales can be effectively described using a thermal time-chilling model, which can be used to infer the delay or advance of greenup onset in relation to climatic warming at global scale.     

Regional unified model‐based leaf unfolding prediction from 1960 to 2009 across northern China

Using first leaf unfolding data of Salix matsudana, Populus simonii, Ulmus pumila, and Prunus armeniaca, and daily mean temperature data during the 1981–2005 period at 136 stations in northern China, we fitted unified forcing and chilling phenology models and selected optimum models for each species at each station. Then, we examined performances of each optimum local species‐specific model in predicting leaf unfolding dates at all external stations within the corresponding climate region and selected 16 local species‐specific models with maximum effective predictions as the regional unified models in different climate regions. Furthermore, we validated the regional unified models using leaf unfolding and daily mean temperature data beyond the time period of model fitting. Finally, we substituted gridded daily mean temperature data into the regional unified models, and reconstructed spatial patterns of leaf unfolding dates of the four tree species across northern China during 1960–2009. At local scales, the unified forcing model shows higher simulation efficiency at 83% of data sets, whereas the unified chilling model indicates higher simulation efficiency at 17% of data sets. Thus, winter temperature increase so far has not yet significantly influenced dormancy and consequent leaf development of deciduous trees in most parts of northern China. Spatial and temporal validation confirmed capability and reliability of regional unified species‐specific models in predicting leaf unfolding dates in northern China. Reconstructed leaf unfolding dates of the four tree species show significant advancements by 1.4–1.6 days per decade during 1960–2009 across northern China, which are stronger for the earlier than the later leaf unfolding species. Our findings suggest that the principal characteristics of plant phenology and phenological responses to climate change at regional scales can be captured by phenological and climatic data sets at a few representative locations.     

Spatial and temporal variability of the phenological seasons in Germany from 1951 to 1996

Various indications for shifts in plant and animal phenology resulting from climate change have been observed in Europe. This analysis of phenological seasons in Germany of more than four decades (1951–96) has several major advantages: (i) a wide and dense geographical coverage of data from the phenological network of the German Weather Service, (ii) the 16 phenophases analysed cover the whole annual cycle and, moreover, give a direct estimate of the length of the growing season for four deciduous tree species. After intensive data quality checks, two different methods – linear trend analyses and comparison of averages of subintervals – were applied in order to determine shifts in phenological seasons in the last 46 years. Results from both methods were similar and reveal a strong seasonal variation. There are clear advances in the key indicators of earliest and early spring (?0.18 to ?0.23 d y^?1) and notable advances in the succeeding spring phenophases such as leaf unfolding of deciduous trees (?0.16 to ?0.08 d y^?1). However, phenological changes are less strong during autumn (delayed by + 0.03 to + 0.10 d y^?1 on average). In general, the growing season has been lengthened by up to ?0.2 d y^?1 (mean linear trends) and the mean 1974–96 growing season was up to 5 days longer than in the 1951–73 period. The spatial variability of trends was analysed by statistical means and shown in maps, but these did not reveal any substantial regional differences. Although there is a high spatial variability, trends of phenological phases at single locations are mirrored by subsequent phases, but they are not necessarily identical. Results for changes in the biosphere with such a high resolution with respect to time and space can rarely be obtained by other methods such as analyses of satellite data.     

Trends in recent temperature and radial tree growth spanning 2000 years across northwest Eurasia

This paper describes variability in trends of annual tree growth at several locations in the high latitudes of Eurasia, providing a wide regional comparison over a 2000-year period. The study focuses on the nature of local and widespread tree-growth responses to recent warming seen in instrumental observations, available in northern regions for periods ranging from decades to a century. Instrumental temperature data demonstrate differences in seasonal scale of Eurasian warming and the complexity and spatial diversity of tree-growing-season trends in recent decades. A set of long tree-ring chronologies provides empirical evidence of association between inter-annual tree growth and local, primarily summer, temperature variability at each location. These data show no evidence of a recent breakdown in this association as has been found at other high-latitude Northern Hemisphere locations. Using Kendall's concordance, we quantify the time-dependent relationship between growth trends of the long chronologies as a group. This provides strong evidence that the extent of recent widespread warming across northwest Eurasia, with respect to 100- to 200-year trends, is unprecedented in the last 2000 years. An equivalent analysis of simulated temperatures using the HadCM3 model fails to show a similar increase in concordance expected as a consequence of anthropogenic forcing.     

中国东部温带植被生长季节的空间外推估计

利用地面植物物候和遥感归一化差值植被指数（NDVI）数据,以及一种物候-遥感外推方法,实现植被生长季节从少数站点到较多站点的空间外推。结果表明：（1）在1982～1993年期间,中国东部温带地区植被生长季节多年平均起讫日期的空间格局与春季和秋季平均气温的空间格局相关显著;（2）在不同纬度带和整个研究区域,植被生长季节结束日期呈显著推迟的趋势,而开始日期则呈不显著提前的趋势,这与欧洲和北美地区植被生长季节开始日期显著提前而结束日期不显著推迟的变化趋势完全不同;（3）北部纬度带的植被生长季节平均每年延长1．4～3．6d,全区的植被生长季节平均每年延长1．4d,与同期北半球和欧亚大陆植被生长季节延长的趋势数值相近;（4）植被生长季节结束日期的显著推迟与晚春至夏季的区域性降温有关,而植被生长季节开始日期的不显著提前则与晚冬至春季气温趋势的不稳定变化有关;（5）在年际变化方面,植被生长季节开始和结束日期分别与2～4月份平均气温和5～6月份平均气温呈负相关关系。     

Disentangling the paradox of insect phenology: are temporal trends reflecting the response to warming?

The strength and direction of phenological responses to changes in climate have been shown to vary significantly both among species and among populations of a species, with the overall patterns not fully resolved. Here, we studied the temporal and spatial variability associated with the response of several insect species to recent global warming. We use hierarchical models within a model comparison framework to analyze phenological data gathered over 40 years by the Japan Meteorological Agency on the emergence dates of 14 insect species at sites across Japan. Contrary to what has been predicted with global warming, temporal trends of annual emergence showed a later emergence day for some species and sites over time, even though temperatures are warming. However, when emergence data were analyzed as a function of temperature and precipitation, the overall response pointed out an earlier emergence day with warmer conditions. The apparent contradiction between the response to temperature and trends over time indicates that other factors, such as declining populations, may be affecting the date phenological events are being recorded. Overall, the responses by insects were weaker than those found for plants in previous work over the same time period in these ecosystems, suggesting the potential for ecological mismatches with deleterious effects for both suites of species. And although temperature may be the major driver of species phenology, we should be cautious when analyzing phenological datasets as many other factors may also be contributing to the variability in phenology.     

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.     

Does flower phenology mirror the slowdown of global warming?

Although recent global warming trends in air temperature are not as pronounced as those observed only one decade ago, global mean temperature is still at a very high level. Does plant phenology – which is believed to be a suitable indicator of climate change – respond in a similar way, that is, does it still mirror recent temperature variations? We explored in detail long-term flowering onset dates of snowdrop, cherry, and lime tree and relevant spring temperatures at three sites in Germany (1901–2012) using the Bayesian multiple change-point approach. We investigated whether mean spring temperature changes were amplified or slowed down in the past decade and how plant phenology responded to the most recent temperature changes. Incorporating records with different end points (i.e., 2002 and 2012), we compared differences in trends and inferred possible differences caused by extrapolating phenological and meteorological data. The new multiple-change point approach is characterized by an enhanced structure and greater flexibility compared to the one change point model. However, the highest model probabilities for phenological (meteorological) records were still obtained for the one change point (linear) model. Marked warming trends in the recent decade were only revealed for mean temperatures of March to May, here better described with one or two change point models. In the majority of cases analyzed, changes in temperatures were well mirrored by phenological changes. However, temperatures in March to May were linked to less strongly advancing onset dates for lime tree flowering during the period 1901-2012, pointing to the likely influence of photoperiodic constraints or unfulfilled chilling requirements. Due to the slowdown of temperature increase, analyses conducted on records ending in 2002 demonstrated distinct differences when compared with records ending in 2012. Extrapolation of trends could therefore (along with the choice of the statistical method) lead to distinctly different results and most recent data should be integrated in order not to over- or underestimate future phenological changes.     

Comparison of phenology trends by land cover class: a case study in the Great Basin, USA

Direct impacts of human land use and indirect impacts of anthropogenic climate change may alter land cover and associated ecosystem function, affecting ecological goods and services. Considerable work has been done to identify long‐term global trends in vegetation greenness, which is associated with primary productivity, using remote sensing. Trend analysis of satellite observations is subject to error, and ecosystem change can be confused with interannual variability. However, the relative trends of land cover classes may hold clues about differential ecosystem response to environmental forcing. Our aim was to identify phenological variability and 10‐year trends for the major land cover classes in the Great Basin. This case study involved two steps: a regional, phenology‐based land cover classification and an identification of phenological variability and 10‐year trends stratified by land cover class. The analysis used a 10‐year time series of Advanced Very High Resolution Radiometer satellite data to assess regional scale land cover variability and identify change. The phenology‐based regional classification was more detailed and accurate than national or global products. Phenological variability over the 10‐year period was high, with substantial shifts in timing of start of season of up to 9 weeks. The mean long‐term trends of montane land cover classes were significantly different from valley land cover classes due to a poor response of montane shrubland and pinyon‐juniper woodland to the early 1990s drought. The differential response during the 1990s suggests that valley ecosystems may be more resilient and montane ecosystems more susceptible to prolonged drought. This type of regional‐scale land cover analysis is necessary to characterize current patterns of land cover phenology, distinguish between anthropogenically driven land cover change and interannual variability, and identify ecosystems potentially susceptible to regional and global change.     

Advances in first bloom dates and increased occurrences of yearly second blooms in eastern China since the 1960s: further phenological evidence of climate warming

Confirming the results of previous regional studies on changes in first bloom dates (FBD) in China, this study provides evidence that complements conclusions drawn from studies of phenological changes in other dynamic climate systems in the Northern Hemisphere. Furthermore, increased occurrences of yearly second blooms (YSB) further reinforce results derived from other studies indicating a recent trend of generalized climate warming across China. Additionally, ascertaining changes in FBD and YSB against a recent background not only provides a hitherto poorly formulated autumnal equivalent to the well-studied shifts in FBD, but also formulates both spring and autumn flowering changes in recent years. Data in this study are derived from observations made from 1963 to 2006 by the Chinese Phenological Observation Network (CPON)—a nationwide system of monitoring stations that has made observations of over 173 species from across China since 1963. At each site, the mean value of each species’ annual deviation and spring mean surface temperatures were calculated. For each species, years and locations were also recorded for species in which second blooms (YSB) occurred. Of the 46 FBD samples, 31 showed advances from the mean, blooming earlier over the course of the study period. Notably, although only 8 of the 46 FBD samples showed significance levels of 0.1 or better, the average FBD did advance by 5.3 days. After the 1980s, the frequency of YSB occurrence remained steady, declining a little from the peak in the 1980s, but still exhibiting occurrences far more than were observed earlier. The data from this study clearly indicate that both the phenological advance of FBD in spring and the increased occurrence of YSB are consistent with climate warming.     

Future Bloom and Blossom Frost Risk for Malus domestica Considering Climate Model and Impact Model Uncertainties

The future bloom and risk of blossom frosts for Malus domestica were projected using regional climate realizations and phenological ( = impact) models. As climate impact projections are susceptible to uncertainties of climate and impact models and model concatenation, the significant horizon of the climate impact signal was analyzed by applying 7 impact models, including two new developments, on 13 climate realizations of the IPCC emission scenario A1B. Advancement of phenophases and a decrease in blossom frost risk for Lower Saxony (Germany) for early and late ripeners was determined by six out of seven phenological models. Single model/single grid point time series of bloom showed significant trends by 2021–2050 compared to 1971–2000, whereas the joint signal of all climate and impact models did not stabilize until 2043. Regarding blossom frost risk, joint projection variability exceeded the projected signal. Thus, blossom frost risk cannot be stated to be lower by the end of the 21st century despite a negative trend. As a consequence it is however unlikely to increase. Uncertainty of temperature, blooming date and blossom frost risk projection reached a minimum at 2078–2087. The projected phenophases advanced by 5.5 d K⁻¹, showing partial compensation of delayed fulfillment of the winter chill requirement and faster completion of the following forcing phase in spring. Finally, phenological model performance was improved by considering the length of day.     

我国东部北亚热带植物群落季相的时空变化

研究我国东部亚热带植物群落物候与气候变化的关系,对于揭示东部季风区生态系统对气候变化响应的整体特征和空间分异,具有重要的科学意义。作者利用物候累积频率拟合法对盐城、武汉、合肥、屯溪1982-1996年的植物群落季相阶段进行划分,并分析了季相阶段的时空变化及其与气温的统计关系。结果表明：（1）各站多年平均变绿期、旺盛光合期和休眠期初日均有随海拔升高而推迟的倾向,而多年平均季相阶段长度的空间分异特征不明显。休眠期初日随海拔升高而推迟的事实表明,树木秋季叶变色和落叶除受到气温的影响外,还可能与光照和霜等其它环境因素有关,从而使得海拔升高对秋季物候期提早的影响有所削弱,其生态机制有待进一步研究。（2）各站变绿期初日以提前为主,长度以延长为主;旺盛光合期和凋落期初日均以提前为主,长度延长与缩短参半;休眠期初日提前与推迟参半,长度以缩短为主。（3）各站变绿期和旺盛光合期初日与前期平均气温多呈显著负相关,而凋落期和休眠期初日与前期平均气温相关不显著。利用最佳时段气温-物候回归模型重建的1982-2006年季相阶段初日的时间序列显示,盐城、武汉和屯溪的变绿期初日呈显著提前的趋势,盐城、合肥和武汉旺盛光合期初日也呈显著提前的趋势。值得注意的是,在2002-2006年期间,各站变绿期和旺盛光合期初日均表现出明显推迟的倾向,与各地该时段前期平均气温呈下降的倾向一致。（4）从北亚热带各站到温带北部的哈尔滨,平均每向北1个纬度,多年平均变绿期和旺盛光合期初日分别显著推迟2.7-4.0 d和1.8-2.8 d,而长度则多呈不显著缩短的趋势;凋落期初日提前不显著,但长度显著缩短1.8-2.6 d;休眠期初日显著提前2.9-3.3 d,且长度显著延长5.8-7.0 d。总体上看,上述观测事实符合植物物候空间变化的一般规律,即在生长季节前半段,低纬地区的植物物候早于高纬地区;在生长季节后半段,高纬地区的植物物候早于低纬地区。     

Observed changes in winter wheat phenology in the North China Plain for 1981–2009

Climate change in the last three decades could have major impacts on crop phenological development and subsequently on crop productivity. In this study, trends in winter wheat phenology are investigated in 36 agro-meteorological stations in the North China Plain (NCP) for the period 1981–2009. The study shows that the dates of sowing (BBCH 00), emergence (BBCH 10) and dormancy (start of dormancy) are delayed on the average by 1.5, 1.7 and 1.5 days/decade, respectively. On the contrary, the dates of greenup (end of dormancy), anthesis (BBCH 61) and maturity (BBCH 89) occur early on the average by 1.1, 2.7 and 1.4 days/decade, respectively. In most of the investigated stations, GP2 (dormancy to greenup), GP3 (greenup to anthesis) and GP0 (entire period from emergence to maturity) of winter wheat shortened during the period 1981–2009. Due, however, to early anthesis, grain-filling stage occurs at lower temperatures than before. This, along with shifts in cultivars, slightly prolongs GP4 (anthesis to maturity). Comparison of field-observed CERES (Crop Environment Resource Synthesis)-wheat model-simulated dates of anthesis and maturity suggests that climate warming is the main driver of the changes in winter wheat phenology in the NCP. The findings of this study further suggest that climate change impact studies should be strengthened to adequately account for the complex responses and adaptations of field crops to this global phenomenon.     

Shifts in the temperature‐sensitive periods for spring phenology in European beech and pedunculate oak clones across latitudes and over recent decades

Spring phenology of temperate trees has advanced worldwide in response to global warming. However, increasing temperatures may not necessarily lead to further phenological advance, especially in the warmer latitudes because of insufficient chilling and/or shorter day length. Determining the start of the forcing phase, that is, when buds are able to respond to warmer temperatures in spring, is therefore crucial to predict how phenology will change in the future. In this study, we used 4,056 leaf‐out date observations during the period 1969–2017 for clones of European beech (Fagus sylvatica L.) and pedunculate oak (Quercus robur L.) planted in 63 sites covering a large latitudinal gradient (from Portugal ~41°N to Norway ~63°N) at the International Phenological Gardens in order to (a) evaluate how the sensitivity periods to forcing and chilling have changed with climate warming, and (b) test whether consistent patterns occur along biogeographical gradients, that is, from colder to warmer environments. Partial least squares regressions suggest that the length of the forcing period has been extended over the recent decades with climate warming in the colder latitudes but has been shortened in the warmer latitudes for both species, with a more pronounced shift for beech. We attribute the lengthening of the forcing period in the colder latitudes to earlier opportunities with temperatures that can promote bud development. In contrast, at warmer or oceanic climates, the beginning of the forcing period has been delayed, possibly due to insufficient chilling. However, in spite of a later beginning of the forcing period, spring phenology has continued to advance at these areas due to a faster satisfaction of heat requirements induced by climate warming. Overall, our results support that ongoing climate warming will have different effects on the spring phenology of forest trees across latitudes due to the interactions between chilling, forcing and photoperiod.     

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.     

Linking above- and belowground phenology of hybrid walnut growing along a climatic gradient in temperate agroforestry systems

Background and aims

Plant phenology is a sensitive indicator of plant response to climate change. Observations of phenological events belowground for most ecosystems are difficult to obtain and very little is known about the relationship between tree shoot and root phenology. We examined the influence of environmental factors on fine root production and mortality in relation with shoot phenology in hybrid walnut trees (Juglans sp.) growing in three different climates (oceanic, continental and Mediterranean) along a latitudinal gradient in France.

Methods

Eight rhizotrons were installed at each site for 21 months to monitor tree root dynamics. Root elongation rate (RER), root initiation quantity (RIQ) and root mortality quantity (RMQ) were recorded frequently using a scanner and time-lapse camera. Leaf phenology and stem radial growth were also measured. Fine roots were classified by topological order and 0–1 mm, 1–2 mm and 2–5 mm diameter classes and fine root longevity and risk of mortality were calculated during different periods over the year.

Results

Root growth was not synchronous with leaf phenology in any climate or either year, but was synchronous with stem growth during the late growing season. A distinct bimodal pattern of root growth was observed during the aerial growing season. Mean RER was driven by soil temperature measured in the month preceding root growth in the oceanic climate site only. However, mean RER was significantly correlated with mean soil water potential measured in the month preceding root growth at both Mediterranean (positive relationship) and oceanic (negative relationship) sites. Mean RIQ was significantly higher at both continental and Mediterranean sites compared to the oceanic site. Soil temperature was a driver of mean RIQ during the late growing season at continental and Mediterranean sites only. Mean RMQ increased significantly with decreasing soil water potential during the late aerial growing season at the continental site only. Mean root longevity at the continental site was significantly greater than for roots at the oceanic and Mediterranean sites. Roots in the 0–1 mm and 1–2 mm diameter classes lived for significantly shorter periods compared to those in the 2–5 mm diameter class. First order roots (i.e. the primary or parents roots) lived longer than lateral branch roots at the Mediterranean site only and first order roots in the 0–1 mm diameter class had 44.5% less risk of mortality than that of lateral roots for the same class of diameter.

Conclusions

We conclude that factors driving root RER were not the same between climates. Soil temperature was the best predictor of root initiation at continental and Mediterranean sites only, but drivers of root mortality remained largely undetermined.