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.     

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.     

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.     

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.     

An analysis of relationships among plant community phenology and seasonal metrics of Normalized Difference Vegetation Index in the northern part of the monsoon region of China

This study focuses on relationships between the phenological growing season of plant communities and the seasonal metrics of Normalized Difference Vegetation Index (NDVI) at sample stations and pixels overlying them, and explores the procedure for determining the growing season of terrestrial vegetation at the regional scale, using threshold NDVI values obtained by surface–satellite analysis at individual stations/pixels. The cumulative frequency of phenophases has been calculated for each plant community and each year in order to determine the growing season at the three sample stations from 1982 to 1993. The precise thresholds were arbitrarily set as the dates on which the phenological cumulative frequency reached 5% and 10% (for the beginning) and 90% and 95% (for the end). The beginning and end dates of the growing season were then applied each year as time thresholds, to determine the corresponding 10-day peak greenness values from NDVI curves for 8-km² pixels overlying the phenological stations. According to a trend analysis, a lengthening of the growing seasons and an increase of the integrated growing season NDVI have been detected in the central part of the research region. The correlation between the beginning dates of the growing season and the corresponding threshold NDVI values is very low, which indicates that the satellite-sensor-derived greenness is independent of the beginning time of the growing season of local plant communities. Other than in spring, the correlation between the end dates of the growing season and the corresponding threshold NDVI values is highly significant. The negative correlation shows that the earlier the growing season terminates, the larger the corresponding threshold NDVI value, and vice versa. In order to estimate the beginning and end dates of the growing season using the threshold NDVI values at sites without phenological data from 1982 to 1993, we calculated the spatial correlation coefficients between NDVI time-series at each sample station and other contiguous sites year by year. The results provide the spatial extrapolation area of the growing season for each sample station. Thus, we can use the threshold NDVI value obtained at one sample station/pixel for a year to determine the growing season at the extrapolation sites with a similar vegetation type for the same year. Received: 25 October 2000 / Revised: 19 June 2001 / Accepted: 19 June 2001     

Effects of irradiance on growth and flowering in the shade plant, cineraria

Effects of total irradiance on growth and flowering were studied in cineraria cv. Cindy Blue grown under warm (mean 21°C) glasshouse conditions. Efficiency of light conversion for leaf and shoot dry weight increase were reduced from 0.08 to 0.02 as the mean daily light integral increased from 0.9 to 4.4 MJ m^-2 day^-1 but no significant difference in leaf area were associated with this. Specific leaf area decreased exponentially from 0.07 to 0.02 m²g¹ over the cumulative irradiance range 23 to 127 MJ m^-2 after the start of treatments and thereafter remained stable. A light integral of 19.2 MJ m^-2 were required for initiation of one leaf in plants grown under a daily integral of 4.4 MJ m^-2 day^-1, as compared with only 5.1 MJ m^-2day^-1 required per leaf in plants grown at less than 0.9 MJ m^-2day^-1. Neither chronological duration of juvenile development nor leaf number below the flower was affected by irradiance. However, as the rate of leaf initiation increased with irradiance up to 2.4 MJ m^-2day^-1 so the rate of progress to flower visibility increased linearly with irradiance over the same range. This rate then remained constant from 2.4 to 4.4 MJ m^-2day^-1. Length of the main flowering shoot decreased and the number of flowering shoots increased as irradiance increased from 0.9 to 2.4 MJ m^-2 day^-1 and then remained unchanged by further increases in irradiance.     

Determining the growing season of land vegetation on the basis of plant phenology and satellite data in Northern China

The objectives of this study are to explore the relationships between plant phenology and satellite-sensor-derived measures of greenness, and to advance a new procedure for determining the growing season of land vegetation at the regional scale. Three phenological stations were selected as sample sites to represent different climatic zones and vegetation types in northern China. The mixed data set consists of occurrence dates of all observed phenophases for 50–70 kinds of trees and shrubs from 1983 to 1988. Using these data, we calculated the cumulative frequency of phenophases in every 5-day period (pentad) throughout each year, and also drew the cumulative frequency distribution curve for all station-years, in order to reveal the typical seasonal characteristics of these plant communities. The growing season was set as the time interval between 5% and 95% of the phenological cumulative frequency. Average lengths of the growing season varied between 188 days in the northern, to 259 days in the southern part of the research region. The beginning and end dates of the surface growing season were then applied each year as time thresholds, to determine the corresponding 10-day peak greenness values from normalized difference vegetation index curves for 8-km² pixels overlying the phenological stations. Our results show that, at the beginning of the growing season, the largest average greenness value occurs in the southern part, then in the northern, and finally the middle part of the research region. In contrast, at the end of the growing season, the largest average greenness value is measured in the northern part, next in the middle and lastly the southern part of the research region. In future studies, these derived NDVI thresholds can be applied to determine the growing season of similar plant communities at other sites, which lack surface phenological data. Received: 29 November 1999 / Revised: 14 March 2000 / Accepted: 15 March 2000     

Anthesis effects on Posidonia oceanica (L.) Delile phenology in the Bay of Calvi (Corsica,Mediterranean Sea)

In Posidonia oceanica (L.) Delile, anthesis induces a decrease in the number of juvenile leaves resulting in a significant reduction in the number of leaves on the flowering shoots. All the leaves of the flowering shoots are narrower than the leaves of nonflowering shoots. A modification of the leaf growth also appears in flowering shoots: the oldest leaves are longer and the leaves induced during or after anthesis are shorter. At 10 m depth, in the Bay of Calvi, anthesis lasts roughly 3 months and the flowering is induced 7 months before anthesis.     

Pollinators, flowering phenology and floral longevity in two Mediterranean Aristolochia species, with a review of flower visitor records for the genus

The pollination of Aristolochia involves the temporary confinement of visitors inside the flower. A literature review has shown that some species are visited by one or a few dipteran families, while others are visited by a wider variety of dipterans, but only some of these are effective pollinators. We observed flowering phenology and temporal patterns of pollinator attendance in diverse populations of Aristolochia baetica and A. paucinervis, two species that grow in SW Spain, frequently in mixed populations. The two species had overlapping floral phenologies, extended flowering periods and long-lived flowers. A. baetica attracted a higher number of visitors than A. paucinervis . Drosophilids and, to a lesser extent, phorids, were the main pollinators of A. baetica, whereas in A. paucinervis , phorids were the only pollinators. Attendance to A. paucinervis flowers by phorids in mixed populations was markedly lower than in pure populations. This effect was more evident in years with lower pollinator density. Our results suggest that A. baetica and A. paucinervis may compete for pollinators in mixed populations.     

Relationships between phenology and the remobilization of nitrogen, phosphorus and potassium in branches of eight Mediterranean evergreens

Few studies have examined the effects of plant growth on nutrient remobilization in phenologically contrasting species. Here we evaluated the consequences of above-ground seasonality of growth and leaf shedding on the remobilization of nutrients from branches in eight evergreen Mediterranean phanaerophytes that differ widely in phenology. Vegetative growth, flower bud formation, flowering, fruiting, leaf shedding, and the variations in nitrogen (N), phosphorus (P) and potassium (K) pools in branches throughout the year were monitored in each species. Nitrogen and P remobilization occurred in summer, after vegetative growth and synchronously with leaf shedding. Despite the time-lag between growth and remobilization, the branches that invested more nutrients in vegetative growth also remobilized more nutrients from their old organs. Potassium remobilization peaked in the climatically harshest periods, and appears to be related to osmotic requirements. We conclude that N and P remobilization occurs mainly associated with leaf senescence, which might be triggered by factors such as the replenishment of nutrient reserves in woody organs, the hormonal relations between new and old leaves, or the constraints that summer drought poses on the amount of leaf area per branch in summer.     

Factors governing the spatial and temporal distribution of Chironomid larvae in the Maarsseveen lakes with special emphasis on the role of oxygen conditions

Distribution patterns of the larvae of Chironomidae are compared in three water systems in The Netherlands, which vary in trophic state and oxygen regimes. The life cycles and flying periods of some dominant chironomid species in two of the investigated lakes, Lakes Maarsseveen I and II, are determined by comparing data on the seasonal variations in larval densities with existing literature on Chironomidae in the Maarsseveen lakes. In the oligo-mesotrophic Lake Maarsseveen I (LM I), hypoxic or anoxic conditions in the hypolimnion are observed only at the end of the stratification period. A clear zonation of the chironomid fauna is present in this lake. The littoral zone is dominated byCladotanytarsus gr.mancus andStictochironomus sticticus, the littoriprofundal zone byTanytarsus bathophilus, and the profundal zone byChironomus anthracinus. In comparison with the other species in LM I,T. bathophilus larvae show the most variable distribution patterns over time. Larvae are found in all depths from July to September, but disappear from the hypolimnion as soon as oxygen conditions deteriorate. In the eutrophic Lake Maarsseveen II (LM II), oxygen depletion of the hypolimnion starts immediately after the onset of the thermal stratification in June, and continues until autumnal turnover in November. In this lake, the chironomid community consists primarily ofS. sticticus andCl. gr.mancus, and is confined to the narrow littoral zone. No chironomid larvae are found in the deeper parts of the lake. The eutrophic Lake Gijster in the Brabantse Biesbosch is a deep, man-made reservoir, that is artificially destratified during the summer. In this lakeTanytarsus bathophilus is found in the profundal sediments, whereas almost noChironomus is found in this zone. It is concluded that oxygen conditions existing in the deeper regions of the investigated lakes in large part determine the occurrence and distribution of chironomid species. The distribution ofT. bathophilus is limited by unfavorable oxygen conditions and not by the trophic state of the lake. These findings are part of a thesis (HEINIS, 1993).     

Long-term changes in the woodlands of Clairinsh

Summary

The mixed oak woodland on the island of Clairinsh has been left unmanaged as part of the Loch Lomond National Nature Reserve. Until 1913 the woodlands had been treated as coppice-with-standards. Between 1961 and 1986 changes in the structure and composition of the stand were recorded by means of two transects, within which individual trees and shrubs were charted and measured. Most of the stand remained closed, increasing in basal area, but decreasing in density. However, a limited number of canopy gaps formed, part-icularly as a result of the 1968 hurricane. Of the individuals present in 1961, 30% died by 1986, mortality being particularly high in smaller individuals and in birch. Recruitment was mainly confined to rowan, holly and hazel in the closed woodland, and to birch and rowan in the gaps. The changes are discussed in relation to natural processes and the history of management.     

Phenological features in relation to growth forms and biomass accumulation in an alpine meadow of the Central Himalaya

Phenological records of 50 plant species were made during 1988–89 in an alpine meadow (30° 10-30° 13 N lat. and 79° 39-79°-41 E long.) of Central Himalaya located between 3100–3750 m elevation. The growth initiation occurred when temperature began to rise continuously and the resulting in snowmelt. The peaks of the various phenophases succeeded one after another in time, within a period of about four months (from May to September) which is longer than the period reported for the alpine sites of higher latitudes. The period of growth initiation appeared to be related to growth form, the species showing earlier growth initiation (when temperatures were lower) deployed leaves to lower heights, close to the ground. A majority of forbs completed growth cycle earlier than the grasses. For example, one group represented by Trachydium roylei reached peak growth a few weeks before did another group of species, represented by Danthonia cachemyriana, which is indicative of niche separation of the respective group of species. Activities of accumulation of live and dead shoot biomass were clearly separated in time in most communities, the former occurring from May to August, and the latter mainly in September. Nomenclature: Osmaston (1926).     

Latitudinal variation in the fruiting phenology of a bird-dispersed plant (shape Crataegus monogyna) in Western Europe

A number of fleshy-fruit-bearing plants of temperate regions are dispersed by migratory frugivorous birds. It has been suggested that the more southerly populations of such species should produce ripe fruits later than more northerly populations, to ensure that fruit is available when the birds arrive. I will call this the adaptive delay hypothesis. To test this hypothesis, I monitored fruiting phenology of Crataegus monogyna Jacq. at ten sites (in all of which fruit consumption is very largely by redwings, Turdus iliacus, and fieldfares, Turdus pilaris) between northern Spain (42° N) and northern Scotland (59° N). There was no negative correlation between latitude and date of fruit ripening (earliest recorded date on which ripe fruits had appeared, or earliest recorded date by which all fruits had ripened). My results thus argue against the adaptive delay hypothesis.