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.     

Changed plant and animal life cycles from 1952 to 2000 in the Mediterranean region

The available data on climate over the past century indicate that the earth is warming. Important biological effects, including changes of plant and animal life cycle events, have already been reported. However, evidence of such effects is still scarce and has been mostly limited to northern latitudes. Here we provide the first long‐term (1952–2000) evidence of altered life cycles for some of the most abundant Mediterranean plants and birds, and one butterfly species. Average annual temperatures in the study area (Cardedeu, NE Spain) have increased by 1.4 °C over the observation period while precipitation remained unchanged. A conservative linear treatment of the data shows that leaves unfold on average 16 days earlier, leaves fall on average 13 days later, and plants flower on average 6 days earlier than in 1952. Fruiting occurs on average 9 days earlier than in 1974. Butterflies appear 11 days earlier, but spring migratory birds arrive 15 days later than in 1952. The stronger changes both in temperature and in phenophases timing occurred in the last 25 years. There are no significant relationships among changes in phenophases and the average date for each phenophase and species. There are not either significant differences among species with different Raunkiaer life‐forms or different origin (native, exotic or agricultural). However, there is a wide range of phenological alterations among the different species, which may alter their competitive ability, and thus, their ecology and conservation, and the structure and functioning of ecosystems. Moreover, the lengthening of plant growing season in this and other northern hemisphere regions may contribute to a global increase in biospheric activity.     

Climate change fingerprints in recent European plant phenology

A paper published in Global Change Biology in 2006 revealed that phenological responses in 1971–2000 matched the warming pattern in Europe, but a lack of chilling and adaptation in farming may have reversed these findings. Therefore, for 1951–2018 in a corresponding data set, we determined changes as linear trends and analysed their variation by plant traits/groups, across season and time as well as their attribution to warming following IPCC methodology. Although spring and summer phases in wild plants advanced less (maximum advances in 1978–2007), more (~90%) and more significant (~60%) negative trends were present, being stronger in early spring, at higher elevations, but smaller for nonwoody insect‐pollinated species. These trends were strongly attributable to winter and spring warming. Findings for crop spring phases were similar, but were less pronounced. There were clearer and attributable signs for a delayed senescence in response to winter and spring warming. These changes resulted in a longer growing season, but a constant generative period in wild plants and a shortened one in agricultural crops. Phenology determined by farmers’ decisions differed noticeably from the purely climatic driven phases with smaller percentages of advancing (~75%) trends, but farmers’ spring activities were the only group with reinforced advancement, suggesting adaptation. Trends in farmers’ spring and summer activities were very likely/likely associated with the warming pattern. In contrast, the advance in autumn farming phases was significantly associated with below average summer warming. Thus, under ongoing climate change with decreased chilling the advancing phenology in spring and summer is still attributable to warming; even the farmers’ activities in these seasons mirror, to a lesser extent, the warming. Our findings point to adaptation to climate change in agriculture and reveal diverse implications for terrestrial ecosystems; the strong attribution supports the necessary mediation of warming impacts to the general public.     

Phenological responses to extreme droughts in a Mediterranean forest

Mediterranean regions are projected to experience more frequent, prolonged and severe drought as a consequence of climate change. We used a retractable rainfall shelter, to investigate the impact of extreme droughts on the development of Quercus ilex leaves, flowers and fruit. In 2008, 97% of rainfall was excluded from a forest plot during the autumn, representing 50% of the 1127 mm of rain that fell during the year. In 2009, 87% of rainfall was excluded during the spring, representing 58% of the 749 mm that fell during the year. The rainfall shelter did not impact neither incident radiation nor air temperature. Autumn rainfall exclusion did not significantly affect leaf, flowers or fruit development. Spring rainfall exclusion resulted in larger and more sustained depression of leaf water potential during the key phases of foliar and floral development. Consequently, only half of the sampled trees (6) reached the shoot lengthening stage which leads to functionally mature leaves (phenophase 4), with one abandoning leaf development at budburst (phenophase 3) and the other two at the bud swelling stage (phenophase 2). All trees of the control plot passed phenophase 4, with most reaching complete leaf development. The impact of extreme droughts on flower development differed between the sexes. The spring exclusion had no effect on male flower, but only one of six trees completed female fruit maturation, compared with four in the control plot. The difference between the male and female drought impacts is likely attributable to the occurrence of male floral development before the period of lowest leaf water potential, and to the lower resource allocation requirements of male flowers. The information provided by our experimental approach may constitute a crucial step to evaluate the impact of increasing drought due to climate change on the most dominant Mediterranean tree species and to help drawing a full picture of the ecological consequences of the decline in water resource on forest dynamics under changing conditions.     

Cattle change plant reproductive phenology,promoting community changes in a post-fire Nothofagus forest in northern Patagonia,Argentina

Aims Variations in rates and length of flowering and fruiting not only affect the reproduction of a given plant species but also the behavior and reproduction of associated taxa. Flowering and fruiting variations may be influenced by herbivory, especially by large mammals. The aim of this study was to determine the effects of cattle browsing on the reproductive phenology of understory species in a subalpine post-fire Nothofagus forest in Patagonia.Methods The effects of herbivory on plant reproductive phenology were studied in a set of experimental exclosures (fenced plots) installed since 2001 in a post-fire N. pumilio forest, located in Nahuel Huapi National Park (NHNP), Argentina. We monitored the beginning and duration of each reproductive phenological stage: floral bud, open flower, immature fruit and mature fruit. We also counted the number of flowers, fruits, seeds and viable seeds of the dominant plants to assess whether browsing modifies temporal patterns of the flowering and fruiting periods.Important findings Cattle reduced the total number of species flowering and fruiting and changed the reproductive phenology of some species. We found that palatable species seem to be negatively affected by browsing in terms of reduced fitness due to changes in flowering and fruiting periods. In contrast, cattle benefitted the reproduction of non-palatable species and could promote the invasion of shade-intolerant exotic forbs such as Cirsium vulgare. The effects of livestock reported in this study are important to understanding how browsing could alter native species establishment and possibly alter successional trajectories during recolonization after fire.     

Reproductive phenology of a wet forest understorey in the Western Ghats, South India

The reproductive phenology of 60 understorey species was monitored at monthly intervals for 20 months in a medium elevation wet evergreen forest in the Southern Western Ghats. The life forms monitored were herbs (including terrestrial orchids), shrubs and small trees. Flowering and fruiting were non‐uniform with a dry season flowering peak and wet season fruiting peak. Flowering in the understorey correlated negatively with rainfall. No significant correlation was detected for fruiting. Life forms had flowering and fruiting peaks at different times of the year.     

Seasonality in the equatorial tropics: Flower,fruit, and leaf phenology of montane trees in the highlands of Southwest Uganda

Phenology influences many forest functions and can inform forest conservation and management, yet representative phenological data for most common tropical forest tree species remain sparse or absent. Between June 2011 and December 2013, we investigated flowering, fruiting, and leafing patterns in the Bwindi Impenetrable National Park, a montane forest located near the equator in Uganda, drawing on 16,410 observations of 530 trees of 54 species located between 2066 and 2527 m in elevation. The park's climate is equatorial with two wet and dry seasons each year. Flowering and fruiting were strongly seasonal while patterns in leafing were less pronounced. Flower occurrence peaked at the beginning of the short dry season followed by a pronounced trough during the beginning and the middle of the short wet season. Fruit occurrence had a pronounced peak during high rainfall months in March through April with most fruits ripening during drier months in May through July. Fruit scarcity was observed for a 4-month period spanning September to December and most flushing of leaves noted at the end of the wet season in November and December. Our binomial generalized linear mixed models indicated that flowering and fruiting were negatively associated with temperature and that leafing activity was positively associated with rainfall and temperature. These findings are consistent with the insolation- and water-limitation hypotheses suggesting that the seasonally varying availability of resources such as light, water, and nutrients determines these phenological patterns. Ideally, prolonged, multi-year community-level studies would be supported so as to better characterize the influence of climate and of climate variability.     

生殖物候与草甸草地多年生植物的消长

尽管草地管理研究较多,但从物候学进行的研究很少.目前尚未见到关于开花期和结实期如何影响科尔沁草原植物地位的报道.报道了科尔沁草甸草原34种多年生植物的始花期和果实始成熟期与其在割草和放牧利用下的消长关系.结果表明：（1）3种植物在4月、13种在5月、10种在6月、7种在7月、1种在8月开始开花.3种在5月、14种在6月、11种在7月、5种在8月、1种在9月开始出现成熟果实.（2）与割草草地相比,始花期晚的植物在自由放牧草地中频度和多度趋于减少,果实始成熟期晚的植物也表现同样的趋势.（3）当将具有营养繁殖能力的植物排除后,与割草草地相比,始花期和果实始成熟期晚的植物在自由放牧草地中频度和多度减少的趋势更强.（4）为了使植物完成生活史,割草应在秋季大多数植物结实期结束时实施.（5）为保证大多数禾本科植物顺利完成生活史,应在大多数植物开始分蘖时开始放牧,进入花蕾期停止放牧,至结实期晚期又开始放牧.     

Diversity of flowering and fruiting phenology of trees in a tropical deciduous forest in India

BACKGROUND AND AIMS: In the dry tropics, vegetative phenology varies widely with tree characteristics and soil conditions. The present work aims to document the phenological diversity of flowering and fruiting with reference to leafing events in Indian dry-tropical tree species. METHODS: Nine tree species, including one leaf-exchanging and eight deciduous showing varying leafless periods, were studied. Monthly counts of leaves, flowers and fruits were made on 160 tagged twigs on ten individuals of each species for initiation, completion and duration of different phenological events through two annual cycles. KEY RESULTS: Variation in flowering relative to leaf flushing (which occurred just prior to or during a hot, dry summer) revealed five flowering types: summer flowering (on foliated shoots), rainy-season flowering (on foliated shoots following significant rains), autumn flowering (on shoots with mature leaves), winter flowering (on shoots undergoing leaf fall) and dry-season flowering (on leafless shoots). Duration of the fruiting phenophase was shortest (3-4 months) in dry-season and winter-flowering species, 6-9 months in rainy-and autumn-flowering species, and maximum (11 months) in summer-flowering species. A wide range of time lag (<1 to >8 months) between the start of vegetative (first-leaf flush) and reproductive (first-visible flower) phases was recorded in deciduous species; this time lag was correlated with the extent of the leafless period. A synthesis of available phenological information on 119 Indian tropical trees showed that summer-flowering species were most abundant (56 % of total species) amongst the five types recognized. CONCLUSIONS: The wide diversity of seasonal flowering and fruiting with linkages to leaf flush time and leafless period reflect the fact that variable reproductive and survival strategies evolved in tree species under a monsoonic bioclimate. Flowering periodicity has evolved as an adaptation to an annual leafless period and the time required for the fruit to develop. The direct relationship between leafless period (inverse of growing period) and time lag between onset of vegetative and reproductive phases reflects the partitioning of resource use for supporting these phases. Predominance of summer flowering coupled with summer leaf flushing seems to be a unique adaptation in trees to survive under a strongly seasonal tropical climate.     

芦芽山针叶林分布上下限土壤温度及含水量的季节差异

山地小气候特征对解释林线位置、形成机制以及生长-气候关系具有重要意义。由于高山气象数据匮乏,尤其是土壤水热数据的缺失,使以往对华北地区山地土壤的温湿度变化特征知之甚少。基于5个整年(2012—2016年)的连续监测,分析了华北芦芽山针叶林分布上下限土壤(10cm)温度和含水量的季节变化特征及差异。结果表明:(1)在芦芽山针叶林分布上限,北坡土壤10月末冻结,5月初解冻,南坡土壤冻结和解冻日均滞后于北坡,生长季内南北坡土壤均温、生长季长度无显著差异(122d,8.1℃和110d,7.6℃);(2)南北坡林线土壤含水量最低值都出现在冬季(1月),最高值则在秋季(10月和9月),并且南坡生长季土壤含水量(0.350 m³/m³)显著大于北坡(0.247 m³/m³);(3)与针叶森林的分布下限(2040 m a.s.l.)相比,林线土壤热量指标(年均温、生长季均温、最热月均温和生长季长度)均明显偏低,而土壤生长季内含水量显著偏大。研究结果揭示了亚高山区土壤冻融过程中温度和含水量的耦合关系,并进一步证实了芦...     

青藏高原草地主要单子叶植物的叶表面特征

采用光学显微镜对青藏高原草地主要单子叶植物的叶表面特征进行观测,并运用one-way ANOVA、Pearson相关及线性回归分析,研究了气孔数量指标的物种间差异性以及气孔数量特征与海拔、生长季均温及生长季降水之间的关系。结果表明:(1)青藏高原草地主要单子叶植物长期受高原气候环境的筛选,形成了一些特有的叶表面共性特征,(a)叶表面细胞有长细胞与短细胞两种类型。长细胞呈规则长方形,排列紧密,纵向相接成行;短细胞呈长方形、方形、近圆形或马鞍形,随机散生、单生或孪生,短细胞形态与分布方式因植物种类而异。(b)气孔多分布于叶片下表面,属于单面分布型气孔。气孔选择性地分布在下表面,可在不影响CO_2同化率的情况下,一定程度上起到限制水分蒸发,避免造成生理干旱的作用。(c)不同物种气孔器形态、保卫细胞及副卫细胞形态表现出较为明显的多态性。保卫细胞近方形、半月形或哑铃形;副卫细胞呈低圆顶形、圆顶形或高圆顶形;气孔器为椭圆形、宽椭圆形或近圆形。(d)气孔器类型均是平列型(paracytic type),由两个副卫细胞与保卫细胞共同构成;副卫细胞与保卫细胞平行,并完全包围保卫细胞。气孔器等间距或不等间距呈直线排列形成"气孔带"。(2)青藏高原草地单子叶植物叶表面的气孔密度(SD)较大,平均为(194.07±4.74)个/mm~2,气孔长度(SL)较小(34.50±0.28)μm,气孔指数(SI)为(18.13±0.31)%,其中SD的变异系数(CV)最大(53.02%),SI的变异系数次之(37.23%),SL的变异系数最小(17.94%)。不同物种间叶表面的SL、SD与SI差异极显著(P0.01)。(3)青藏高原草地单子叶植物叶表面气孔数量特征与环境生态因子显著相关。海拔与叶表面气孔特征呈显著正相关(P0.01),生长季均温与SL之间呈弱正相关(P0.05),与SD、SI之间呈显著负相关(P0.01),生长季降水与SL之间呈显著负相关(P0.01)。具体表现为随海拔升高SL、SD与SI增加,随生长季均温降低SL减小、SD与SI显著增大,而随着生长季降水减少SL变大、SD与SI显著降低。(4)海拔、生长季均温与生长季降水对SL、SD与SI的回归方程分别为Y=0.005X_1+0.878X_2-0.021X_3+12.278、Y=0.046X_1-11.688X_2+0.466X_3-46.391与Y=0.003X_1-0.363X_2+0.009X_3+7.394,回归方程统计检验显著(P0.01);环境生态因子对SD的决定系数最大(R=0.690),SL次之(R=0.557),而对SI的贡献率(R=0.342)相对最小。     

青藏高原草地植物叶解剖特征

运用常规石蜡制片技术对我国青藏高原66种草地植物优势种的叶解剖特征进行研究,并分析了叶解剖特征与海拔、生长季降水及生长季均温之间的关系.结果表明:青藏高原草地植物叶片具有很多适应高寒环境的结构特征,如表皮层厚且表皮细胞大小差异显著,表皮毛等表皮附属物发达,异细胞丰富,通气组织普遍发达等;叶片各组成部分厚度的变异程度不同,其中海绵组织厚度变异最大,其次为上角质层、下表皮层、下角质层、上表皮层、栅栏组织,叶片厚度的变异最小;青藏高原草地植物叶片各组成部分的厚度存在协同进化,上下角质层厚度呈强烈正相关,海绵组织厚度与叶片厚度相关性最强;青藏高原草地植物叶片各组成部分的厚度与海拔、生长季降水、生长季均温3个重要环境变量呈较弱的相关性,总体表现为随海拔升高叶片各组成部分的厚度减小,而随生长季降水和生长季均温的增加叶片厚度增加.     

Long-term changes in breeding phenology at two seabird colonies in the western North Sea

There is compelling evidence that the breeding phenology of many species has changed substantially in recent decades. However, taxonomic and spatial variation in the direction and rate of change is still not well understood. We explored these issues by analysing a dataset containing information on first egg dates of 10 species of seabird at two major breeding colonies (86 km apart) in the western North Sea over a period of 35 years. Within a species, timing of breeding was positively correlated between the two colonies, suggesting that factors affecting the phenology of these species operated at a regional rather than a colony scale. Comparison of time trends among the species revealed contrasting patterns, with some showing no systematic change, others becoming earlier and others later. The clearest species groupings appeared to be among the terns with arrival and/or first egg dates becoming earlier in Arctic Terns Sterna paradisaea , Common Terns Sterna hirundo and Sandwich Terns Sterna sandvicensis , and among the auks (Common Guillemot Uria aalge , Razorbill Alca torda and Atlantic Puffin Fratercula arctica ) and Black-legged Kittiwake Rissa tridactyla where the trend was in the opposite direction towards later breeding. This general trend towards later breeding in the latter group of species contrasts with correlational evidence from many other organisms indicating that breeding phenology is advancing in response to climate change.     

Spring phenology rather than climate dominates the trends in peak of growing season in the Northern Hemisphere

Shifts in plant phenology regulate ecosystem structure and function, which feeds back to the climate system. However, drivers for the peak of growing season (POS) in seasonal dynamics of terrestrial ecosystems remain unclear. Here, spatial–temporal patterns of POS dynamics were analyzed by solar-induced chlorophyll fluorescence (SIF) and vegetation index in the Northern Hemisphere over the past two decades from 2001 to 2020. Overall, a slow advanced POS was observed in the Northern Hemisphere, while a delayed POS distributed mainly in northeastern North America. Trends of POS were driven by the start of growing season (SOS) rather than pre-POS climate both at hemisphere and biome scale. The effect of SOS on the trends in POS was the strongest in shrublands while the weakest in evergreen broad-leaved forest. These findings highlight the crucial role of biological rhythms rather than climatic factors in exploring seasonal carbon dynamics and global carbon balance.     

Responses of canopy duration to temperature changes in four temperate tree species: relative contributions of spring and autumn leaf phenology

While changes in spring phenological events due to global warming have been widely documented, changes in autumn phenology, and therefore in growing season length, are less studied and poorly understood. However, it may be helpful to assess the potential lengthening of the growing season under climate warming in order to determine its further impact on forest productivity and C balance. The present study aimed to: (1) characterise the sensitivity of leaf phenological events to temperature, and (2) quantify the relative contributions of leaf unfolding and senescence to the extension of canopy duration with increasing temperature, in four deciduous tree species (Acer pseudoplatanus, Fagus sylvatica, Fraxinus excelsior and Quercus petraea). For 3 consecutive years, we monitored the spring and autumn phenology of 41 populations at elevations ranging from 100 to 1,600 m. Overall, we found significant altitudinal trends in leaf phenology and species-specific differences in temperature sensitivity. With increasing temperature, we recorded an advance in flushing from 1.9 ± 0.3 to 6.6 ± 0.4 days °C⁻¹ (mean ± SD) and a 0 to 5.6 ± 0.6 days °C⁻¹ delay in leaf senescence. Together both changes resulted in a 6.9 ± 1.0 to 13.0 ± 0.7 days °C⁻¹ lengthening of canopy duration depending on species. For three of the four studied species, advances in flushing were the main factor responsible for lengthening canopy duration with increasing temperature, leading to a potentially larger gain in solar radiation than delays in leaf senescence. In contrast, for beech, we found a higher sensitivity to temperature in leaf senescence than in flushing, resulting in an equivalent contribution in solar radiation gain. These results suggest that climate warming will alter the C uptake period and forest productivity by lengthening canopy duration. Moreover, the between-species differences in phenological responses to temperature evidenced here could affect biotic interactions under climate warming.     

Changes in autumn senescence in northern hemisphere deciduous trees: a meta-analysis of autumn phenology studies

Background and Aims Many individual studies have shown that the timing of leaf senescence in boreal and temperate deciduous forests in the northern hemisphere is influenced by rising temperatures, but there is limited consensus on the magnitude, direction and spatial extent of this relationship.Methods A meta-analysis was conducted of published studies from the peer-reviewed literature that reported autumn senescence dates for deciduous trees in the northern hemisphere, encompassing 64 publications with observations ranging from 1931 to 2010.Key Results Among the meteorological measurements examined, October temperatures were the strongest predictors of date of senescence, followed by cooling degree-days, latitude, photoperiod and, lastly, total monthly precipitation, although the strength of the relationships differed between high- and low-latitude sites. Autumn leaf senescence has been significantly more delayed at low (25° to 49°N) than high (50° to 70°N) latitudes across the northern hemisphere, with senescence across high-latitude sites more sensitive to the effects of photoperiod and low-latitude sites more sensitive to the effects of temperature. Delays in leaf senescence over time were stronger in North America compared with Europe and Asia.Conclusions The results indicate that leaf senescence has been delayed over time and in response to temperature, although low-latitude sites show significantly stronger delays in senescence over time than high-latitude sites. While temperature alone may be a reasonable predictor of the date of leaf senescence when examining a broad suite of sites, it is important to consider that temperature-induced changes in senescence at high-latitude sites are likely to be constrained by the influence of photoperiod. Ecosystem-level differences in the mechanisms that control the timing of leaf senescence may affect both plant community interactions and ecosystem carbon storage as global temperatures increase over the next century.     

Exploring the causes of variation in phenology and morphology in Mediterranean geophytes: a genus-wide study of Cyclamen

The phenology and morphology of Mediterranean plants are constrained by drought in summer and cold temperatures in winter. In this study we examine how climatic factors and phylogenetic constraints have shaped variation in the phenology and morphology of 17 species of the genus Cyclamen cultivated in uniform garden conditions. We quantify the extent to which traits differ among subgenera and thus represent conserved traits within evolutionary lineages. We also explore whether leaf, flowering and seed-release phenology are correlated among species, and thus whether variation in flowering phenology results from selection on dispersal phenology. Our results show a significant influence of subgenus membership on leaf and flowering phenology but not on morphological traits or the timing of seed release. Among-species variation in foliage height, leaf size and seed mass (but not in floral traits) is correlated with chromosome number. Leaf traits show that species with a shorter vegetative period have a higher capacity for resource acquisition. Major phenological shifts, i.e. spring vs. autumn flowering and a decoupling of leaf and flower phenology in autumnal flowering species, thus occurred prior to the diversification of species in each subgenus and not as a response to selection on dispersal timing. Leaf and flowering phenology illustrate a gradient of strategies from autumn flowering in the absence of leaves (hysteranthous species) to spring flowering with fully developed foliage (synanthous species). In the former, flowering is uncoupled from resource acquisition by simultaneous photosynthesis, indicative that hysteranthy is a response to temporal unpredictability in the onset of rain after the summer drought. Our results support the idea that whereas leaf development is controlled primarily by moisture availability and secondarily by temperature, flowering is temperature dependent, above a minimum moisture threshold. © 2004 The Linnean Society of London, Botanical Journal of the Linnean Society, 2004, 145 , 469–484.