Variable flowering phenology and pollinator use in a community suggest future phenological mismatch

Recent anthropogenic climate change is strongly associated with average shifts toward earlier seasonal timing of activity (phenology) in temperate-zone species. Shifts in phenology have the potential to alter ecological interactions, to the detriment of one or more interacting species. Recent models predict that detrimental phenological mismatch may increasingly occur between plants and their pollinators. One way to test this prediction is to examine data from ecological communities that experience large annual weather fluctuations. Taking this approach, we analyzed interactions over a four-year period among 132 plant species and 665 pollinating insect species within a Mediterranean community. For each plant species we recorded onset and duration of flowering and number of pollinator species. Flowering onset varied among years, and a year of earlier flowering of a species tended to be a year of fewer species pollinating its flowers. This relationship was attributable principally to early-flowering species, suggesting that shifts toward earlier phenology driven by climate change may reduce pollination services due to phenological mismatch. Earlier flowering onset of a species also was associated with prolonged flowering duration, but it is not certain that this will counterbalance any negative effects of lower pollinator species richness on plant reproductive success. Among plants with different life histories, annuals were more severely affected by flowering–pollinator mismatches than perennials. Specialized plant species (those attracting a smaller number of pollinator species) did not experience disproportionate interannual fluctuations in phenology. Thus they do not appear to be faced with disproportionate fluctuations in pollinator species richness, contrary to the expectation that specialists are at greatest risk of losing mutualistic interactions because of climate change.     

Do changes in rainfall patterns affect semiarid annual plant communities?

Question: Climate change models forecast a reduction in annual precipitation and more extreme events (less rainy days and longer drought periods between rainfall events), which may have profound effects on terrestrial ecosystems. Plant growth, population and community dynamics in dry environments are likely to be affected by these changes since productivity is already limited by water availability. We tested the effects of reduced precipitation and fewer rain events on three semiarid plant communities dominated by annual species. Location: Three semiarid plant communities from Almería province (SE Spain). Methods: Rain‐out shelters were set up in each community and watering quantity and frequency were manipulated from autumn to early summer. Plant productivity, cover and diversity were measured at the end of the experimental period. Results: We found that a 50% reduction in watering reduced productivity, plant cover and diversity in all three communities. However, neither the 25% reduction in watering nor changes in the frequency of watering events affected these parameters. Conclusions: The lack of response to small reductions in water could be due to the identity and resistance of the plant communities involved, which are adapted to rainfall variability characteristic of arid environments. Therefore, a rainfall reduction of 25% or less may not affect these plant communities in the short term, although higher reductions or long‐term changes in water availability would probably reduce productivity and diversity in these communities.     

Two Mediterranean annuals feature high within-population trait variability and respond differently to a precipitation gradient

Intraspecific trait variability plays an important role in species adaptation to climate change. However, it still remains unclear how plants in semi-arid environments respond to increasing aridity. We investigated the intraspecific trait variability of two common Mediterranean annuals (Geropogon hybridus and Crupina crupinastrum) with similar habitat preferences. They were studied along a steep precipitation gradient in Israel similar to the maximum predicted precipitation changes in the eastern Mediterranean basin (i.e. −30% until 2100). We expected a shift from competitive ability to stress tolerance with decreasing precipitation and tested this expectation by measuring key functional traits (canopy and seed release height, specific leaf area, N- and P-leaf content, seed mass). Further, we evaluated generative bet-hedging strategies by different seed traits. Both species showed different responses along the precipitation gradient. C. crupinastrum exhibited only decreased plant height towards aridity, while G. hybridus showed strong trends of generative adaptation to aridity. Different seed trait indices suggest increased bet-hedging of G. hybridus in arid environments. However, no clear trends along the precipitation gradient were observed in leaf traits (specific leaf area and leaf N-/P-content) in both species. Moreover, variance decomposition revealed that most of the observed trait variation (≫50%) is found within populations. The findings of our study suggest that responses to increased aridity are highly species-specific and local environmental factors may have a stronger effect on intraspecific trait variation than shifts in annual precipitation. We therefore argue that trait-based analyses should focus on precipitation gradients that are comparable to predicted precipitation changes and compare precipitation effects to effects of local environmental factors.     

An examination of the relationship between flowering times and temperature at the national scale using long-term phenological records from the UK

This paper examines the mean flowering times of 11 plant species in the British Isles over a 58-year period, and the flowering times of a further 13 (and leafing time of an additional 1) for a reduced period of 20 years. Timings were compared to Central England temperatures and all 25 phenological events were significantly related (P<0.001 in all but 1 case) to temperature. These findings are discussed in relation to other published work. The conclusions drawn from this work are that timings of spring and summer species will get progressively earlier as the climate warms, but that the lower limit for a flowering date is probably best determined by examining species phenology at the southern limit of their distribution. Received: 21 October 1999 / Revised: 27 January 2000 / Accepted: 27 January 2000     

Adaptive phenology of desert and Mediterranean populations of annual plants grown with and without water stress

Summary The dynamics of vegetative and reproductive growth were compared in matched pairs of Mediteranean and desert populations of three unrelated annual species, Erucaria hispanica (L.) Druce, Brachypodium distachyon (L.) Beauv. and Bromus fasciculatus C. Presl., under high and low levels of water availability in a common-environment experiment. Plants of all desert populations showed earlier switches to reproductive development and to subsequent phenophases, and the transition to flowering occurred at smaller plant sizes. Water stress had no effect (E. hispanica) or slightly accelerated the transition to flowering in B. fasciculatus (by 1–2 days) and in B. distachyon (by 4–6 days). Plant senescence was strongly enhanced by water stress, and this enhancement was greater in desert populations than in corresponding Mediterranean ones. Duration of life cycle was greatly shortened by water stress in all three species. Desert and Mediterranean populations of the three species exhibited small differences in their relative response, i.e. phenotypic plasticity, to water stress for phenological and plant size parameters. In E. hispanica and B. fasciculatus the population x water regime interaction amounted to less than 3% of total variance. By contrast, the Mediterranean population of B. distachyon was much more plastic in its response to water stress than the desert population in its transition to plant senescence. Plants from the desert populations appeared to be adapted to shorter, more compact growth cycles, culminating in earlier dates of seed maturation and plant senescence. In addition, they showed larger phenotypic plasticity in the transition to plant senescence, which trait was enhanced or magnified by sustained or repeated lack of water. By contrast, plants from Mediterranean populations delayed switchover from one phenophase to the next, seeming thus to bet on more water being forthcoming.     

Earlier summer drought affects leaf functioning of the Mediterranean species Cistus monspeliensis L.

The Mediterranean vegetation is characterized by a high diversity of growth forms, habits and phenology that enable it to endure under harsh environmental conditions. It is however unclear whether these adaptations may allow plant survival under more extreme conditions, as predicted by climatic models under the perspective of climate change. A manipulative experiment aiming at anticipating summer aridity has been run to analyse the effects of the experimental drought on spring-leaf functioning and characteristics of the leaf-dimorphic Mediterranean shrub Cistus monspeliensis L.Assimilation rates were reduced under anticipated summer aridity due to a decrease of stomatal conductance, but only before morphological adaptations to drought (an increase of leaf mass per area) occurred. These adaptations were anticipated under experimental dry conditions, and causes photosynthetic performances to recover compared to previous dates. When natural summer aridity occurred, the leaf mass per area also changed in the control. However, this causes no recovery of the photosynthetic performances, because of the decrease of stomatal conductance due to low soil water content and leaf water potential values. Moreover, under experimental drought, leaf shedding was anticipated to reduce water losses, causing an overall reduction of leaf lifespan.     

Response of birds to climatic variability; evidence from the western fringe of Europe

Ireland’s geographic location on the western fringe of the European continent, together with its island status and impoverished avifauna, provides a unique opportunity to observe changes in bird migration and distribution patterns in response to changing climatic conditions. Spring temperatures have increased in western Europe over the past 30 years in line with reported global warming. These have been shown, at least in part, to be responsible for changes in the timing of life cycle events (phenology) of plants and animals. In order to investigate the response of bird species in Ireland to changes in temperature, we examined ornithological records of trans-Saharan migrants over the 31-year period 1969–1999. Analysis of the data revealed that two discrete climatic phenomena produced different responses in summer migrant bird species. Firstly, a number of long-distance migrants showed a significant trend towards earlier arrival. This trend was evident in some species and was found to be a response to increasing spring air temperature particularly in the month of March. Secondly, (1) a step change in the pattern of occurrences of non-breeding migrant bird species, and (2) an increase in the ringing data of migrant species were found to correlate with a step change in temperature in 1987–1988. These results indicate that, for migrant bird species, the impact of a sudden change in temperature can be as important as any long-term monotonic trend, and we suggest that the impact of step change events merits further investigation on a wider range of species and across a greater geographical range.     

迁地保育植物花期物候对迁入地气候变化的响应

以中国科学院武汉植物园内栽培的长果秤锤树(Sinojackia dolichocarpa C. J. Qi)、山白树(Sinowilsonia henryi Hemsl.)、夏腊梅(Sinocalycanthus chinensis Cheng et S. Y. Chang)、紫茎(Stewartia sinensis Rehd. et Wils.)和绒毛皂荚(Gleditsia vestita Chun et How ex B. G. Li) 5种迁地保育植物为对象,通过2008-2016年观察记录的初花期物候及整个花期长度的数据,研究花期的年际变化规律及其与迁入地武汉气候因子的相关性。结果显示:(1)从初花期来看,长果秤锤树的初花期每年提前1.25 d,紫茎的初花期每年推迟1.35 d,绒毛皂荚的初花期每年推迟1.22 d。(2)从花期长度来看,山白树的花期每年增加1.72 d,夏蜡梅的花期每年减少1.62 d,紫茎的花期每年增加0.32 d。(3)从花期与气候因子的相关性来看,年降水量、年平均相对湿度、 10℃有效积温、花前 10℃的有效积温是影响这5种植物初花期、花期长度的主要气候因子;不同物种间影响花期的主要气候因子有所差异。     

Growth responses to climate and drought at the southernmost European limit of Mediterranean Pinus pinaster forests

Climate warming and increasing aridity may negatively impact forest productivity across southern Europe. A better understanding of growth responses to climate and drought in southernmost populations could provide insight on the vulnerability of those forests to aridification. Here we investigate growth responses to climate and drought in nine Pinus pinaster (maritime pine) stands situated in Andalusia, southern Europe. The effect of climatic variables (temperatures and precipitation) and drought on radial growth was studied using dendrochronology along biogeographic and ecological gradients. We analyzed old native stands with non-tapped and resin-tapped trees mixed, showing their usefulness in dendroclimatic studies. Our results indicate a high plasticity in the growth responses of maritime pine to climate and drought, suggesting that site aridity modulated these responses. The positive growth responses to spring precipitation and the negative responses to summer drought were stronger in the more xeric inland sites than in wet coastal ones, in particular from the 1980s onwards. The characterization of tree species’ responses to climate at the southern or dry limits in relation to site conditions allows improving conservation strategies in drought-prone forest ecosystems.     

Warming and drought alter soil phosphatase activity and soil P availability in a Mediterranean shrubland

We conducted a field experiment simulating the warming and drought in a Mediterranean shrubland dominated by Erica multiflora and Globularia alypum with the aim to simulate the next future climate conditions predicted by the IPCC and ecophysiological models. As P is frequently a limiting nutrient in Mediterranean ecosystems, we investigated the drought and warming effects on soil phosphatases activities, soil P contents and availability, litter and leaf P concentration, and the capacity of this community to maintain soil P reserves and retain this nutrient in the ecosystem. Warming treatment increased soil and air temperature (an average of 1°C) and drought treatment decreased soil water content in one of the seasons analysed (28% in autum 2004). Warming increased (68%) the activities of soil acid phosphatases in summer and alkaline phosphatase activity (22%) in spring 2004, and increased P concentrations in E. multiflora. Instead, warming decreased P concentrations in litterfall of this same species, E. multiflora, and soil HCO₃-extractable P_i (Olsen-P_i) in some seasons, decreasing total P soil concentration (37%) after 6 years of treatment. The drought treatment did not change soil phosphatase activities, nor available P_i. The effects of climate change on soil P dynamics in Mediterranean areas will thus be strongly dependent on whether the main variable involved in the local change is warming or drought. If warming is the main change without significant changes in water availability, the increases of biological activity can accelerate plant growth, P capture by plants and increase soil-phosphatase activity, altogether decreasing P contents in soil. If drought is the main change, a reduction in P demands by plants is expected, increasing P stocks in soils.     

First approximation to a phenology of the honeybees (Apis mellifera) and flora of Africa

Peak flowering by the total flora of Africa coincides with or immediately follows peak rainfall. Flowering intensity of the total flora decreases with distance from the equator, but that of the honeybee plant resource base (±2% of total flora) does not. Flowering in the latter is highly synchronous (months 1–5 north of and 9–11 south of the equator). Both total and honeybee flora are completely incongruent with either the biomes or phytochoria of Africa. There is no significant correspondence between honeybee phenology and the total flora but significant correspondence occurs between honeybees and flowering in honeybee plant genera. A logistic regression model reveals that honeybee plant flowering predicts major honeybee colony events with a probability of 0.81 south of the equator and 0.71 for the whole continent. It is postulated that promiscuity in the bee plant genera and honeybees of Africa have contributed to their continental ubiquity.     

Tree-ring patterns and climate response of Mediterranean fir populations in Central Greece

Central Greece is the distribution common area of the endemic fir species Abies cephalonica and Abies borisii-regis. Forests fires and fir decline are some of the problems both species encountered during the past decades, with these problems being exacerbated lately by climate change. The present research investigates tree-ring patterns and climate responses of three fir populations along a latitudinal gradient in Central Greece. All three populations were homogeneous in their dendrometric, silvicultural and site characteristics but were phenotypically different. The analysis of tree-ring widths site chronologies revealed that 59% of their variability interprets common tree-ring patterns whereas another 25% interprets their differences as they appear from a south to north direction. This variability in tree-ring widths is proportional to the variability observed for precipitation, temperature and drought from a south to north direction in this region. The tree-ring to climate relationships revealed that the main climatic factor affecting fir tree-ring width is late spring and summer precipitation to which is positively correlated. Also, tree-ring widths were positively affected by the temperatures of the October and April before the growing season. However, June drought adversely affected tree-ring widths of the northern site while it positively affected them at the beginning of the spring season, especially for the southern site and in September for the northern sites. All dendrochronological statistics, tree-ring patterns and climate-growth relationships show a south to north trend following the climatic and phenotypic (species) variation observed to the same direction for fir populations in Central Greece.     

Variability in amount and frequency of water supply affects roots but not growth of arid shrubs

Rainfall and soil moisture variability have a strong effect on plant survival and seed germination in arid environments, yet very little is known about the effects on roots and growth of woody seedlings. Here we focused on the effects of variability in both amount and frequency of water supply on juvenile root and leaf functional traits and growth of seven Mediterranean shrub species occurring in arid SE Spain, Anthyllis cytisoides, Atriplex halimus, Ephedra fragilis, Genista umbellata, Lycium intricatum, Retama sphaerocarpa, and Salsola oppositifolia. In a 14-month greenhouse experiment we manipulated water supply expecting that reduced water amount and pulses of watering of different magnitude affected functional traits and seedling growth, even if the amount of water provided was the same. Different watering patterns altered soil drying dynamics, with reduced supply of water amount and frequent watering becoming the driest treatment. We found that roots of all species responded to alterations in water supply by changing biomass allocation patterns (i.e., higher root-to-shoot mass [R:S] ratio in droughted plants), and by altering fine roots diameter, measured in terms of specific root length. Indeed, differences in growth rate among species were significantly linked to fine roots diameter and biomass allocation, which relates to uptake capacity of roots. However, relative growth rate and leaf traits such as specific leaf area were insensitive, likely because prolonged droughts over longer periods of time seem necessary to constraint growth in all these arid shrubs.     

Forecasting phenology: from species variability to community patterns

Shifts in species' phenology in response to climate change have wide-ranging consequences for ecological systems. However, significant variability in species' responses, together with limited data, frustrates efforts to forecast the consequences of ongoing phenological changes. Herein, we use a case study of three North American plant communities to explore the implications of variability across levels of organisation (within and among species, and among communities) for forecasting responses to climate change. We show how despite significant variation among species in sensitivities to climate, comparable patterns emerge at the community level once regional climate drivers are accounted for. However, communities differ with respect to projected patterns of divergence and overlap among their species' phenological distributions in response to climate change. These analyses and a review of hypotheses suggest how explicit consideration of spatial scale and levels of biological organisation may help to understand and forecast phenological responses to climate change.     

Climate-induced long-term changes in the phenology of Mediterranean fungi

Long-term responses in the phenology of Mediterranean macrofungi to climatic changes are poorly documented. Here, we address this issue by comparing the fruiting patterns of 159 fungal species in Southern France between the first half of the 19th century and the first decade of the 21st century. We used a trait-based approach to assess the influence of phenology and morphology of fungal fruit bodies and their site ecology and biogeography on the response to climate change. We show that early autumnal fruiters, epigeous species and species with affinities for cold climates now start to fruit on average 16.4, 17.3 and 17.3 d later compared to their emergence dates in the 19th century, while late fruiters, hypogeous species and Mediterranean-restricted species did not change their fruiting date. Among ecological guilds, saproxylic species and pine-associated mutualists delayed their autumnal emergence by 32.5 and 19.2 d, likely in response to a delayed rewetting of litter and woody debris after extended summer drought. Our results suggest that long-term climate warming in the Mediterranean was accompanied by contrasting changes in the emergence of fungal fruit bodies according to ecological guilds, sporocarp life-forms and forest types.     

Regional trends for bud burst and flowering of woody plants in Norway as related to climate change

Data series for bud burst, beginning of flowering and petal fall for 20 species of deciduous trees and conifers at four sites in different regions of southern Norway have been analysed and related to temperature series. On average, the spring phenophases occurred 7 days earlier during the period 1971-2005. The most significant linear trends were observed for the earliest phases. The trends in this period were compared with trends in other periods, the longest one starting in 1927. Those starting in cold decades and ending in 2005 were in most instances statistically significant, whereas hardly any significant trend appeared for series starting in warm decades. This fact showed that the results of trend studies are very sensitive to the choice of starting year. There were significant decadal variations in 40% of the series. The dates of occurrence of the phenophases, varying from the first days of May to the first days of June, correlated with seasonal temperature series, in most cases strongest to mean temperatures for the seasons March-May and April-May. The North Atlantic Oscillation Index (NAOI) for January and February appeared to have some predictive power for the date of occurrence of the recorded phases. The basis for this may be that the oscillations described by the index are of importance for the fulfilment of physiological chilling requirements needed to break bud dormancy. The same genotypes of the trees were grown in region West Norway and in Central Norwegian region; during the period 1965-2005 the trends towards earlier bud burst were more pronounced and steeper at the western site.     

Effects of resource availability on plant recruitment at the community level in a Mediterranean mountain ecosystem

Coexisting plant species usually differ in resource requirements, which may also vary within species at successive demographic stages. Such differences become extremely important during the early life stages, since these are the most critical phases in woody-species recruitment, they depend heavily on resources, and they may determine future community composition. Under a global-change scenario, where climatic conditions, nutrient availability, and habitat characteristics are expected to be altered, it is difficult to predict the way in which plant recruitment will be affected. To understand the impact of different global-change drivers on community recruitment, we sowed a set of species representative of the different successional groups of a complete Mediterranean woody community under field conditions, and studied their emergence, growth, and survival along the main resource gradients of light, water, and nutrients. The light and nutrient gradients followed the natural range of conditions in the study area, but water availability was manipulated to simulate three contrasting climatic scenarios: wetter, drier, and current conditions. Structural equation modelling was used to provide a comprehensive analysis of the factors and relations governing plant recruitment. Overall, seedling emergence was determined directly by light; growth was determined by light and summer soil moisture; and survival was determined by summer soil moisture. Light was the main factor indirectly affecting the demographic stages of all species. However, the magnitude of the direct and indirect relationships varied among species. Particularly, species differed in their response to the expected drier climatic conditions, some (e.g. Pinus sylvestris, Acer opalus) being much more vulnerable than others (e.g. Cytisus scoparius, Salvia lavandulifolia). These differential responses could translate as major shifts in the structure of the overall plant community. Our results support the idea that the analysis of complex relations among essential resources is critical for accurate forecasts of the impact of climate change on community dynamics.     

Comparative Physiological and Molecular Analyses of Intraspecific Differences of Stipa purpurea (Poaceae) Response to Drought

Stipa purpurea Griseb, the dominant species of alpine steppe, is widely distributed across the large precipitation gradient on the Tibetan Plateau. It is possible that because of local adaptation, Spurpurea populations from different habitats along this precipitation gradient respond differently to drought, which may affect their responses to climate change. To explore the problem, in the present study, we investigated the physiological and molecular response of Spurpurea seedlings from two different populations (Pulan & Cuoqin) to 14 d drought stress and subsequent recovery. The results showed that the relative water content, chlorophyll fluorescence, content of osmoticant proline and malondialdehyde (indicator of oxidative stress), accumulation of reactive oxygen species, antioxidant enzyme activities and the expression of drought related genes all changed under drought treatment and went back to the control levels in the subsequent recovery in plants from Pulan. However, these patterns were quite different in plants from Cuoqin, in which these traits changed by inconsistent degrees and did not return to pretreatment levels after rewatering. The results demonstrated that the plants from Pulan had greater resistance to drought stress compared with those from Cuoqin, which had a larger mortality rate ultimately. Combating the differences of offspring in response to drought and the habitat distribution of parents, we considered that genetic basis has been obtained in response to precipitation difference among Spurpurea populations. The results help to understand the adaptation and evolution of Spurpurea to the special environment and the effect of climate change to this botanical system.     

Timing of deacclimation affects the ability to recover from simulated winter herbivory

The ability of Vaccinium myrtillus L. to recover from simulated winter herbivory has been investigated on different plants which had been exposed to three elevated temperatures (5 °C, 10 °C or 20 °C) for four weeks in a greenhouse environment. After herbivory, number and length of new aerial shoots and number of leaves/shoot increased faster in plants kept at 5 °C and 10 °C than in those kept at 20 °C. In the following autumn, however, only the shoot number differed between treatments, being greatest in plants of treatments at 5 °C and 10 °C and lowest at 20 °C and the outdoor control. Apparently the plants kept at 20 °C had already used their resources for growth before herbivory simulation, which reduced their recovery ability thereafter. In addition, the growing season was too short for the control plants to produce as many new shoots as the treatments. The results show that the recovery of V. myrtillus from winter herbivory is rapid if it occurs before growth has started. Hence the earlier onset of spring as a consequence of climate warming may not be fatal for the plant, unless the temperature increase triggers growth to start many months earlier than normal.     

Phenology and water relations of tree sprouts and seedlings in a tropical deciduous forest of South India

The phenology of sprouts (>1 year old, up to 1.5 m in height) and seedlings (<1 year old) of six woody species (four deciduous, one brevi-deciduous, and one evergreen) was examined during the dry season in a tropical deciduous forest of South India. Xylem water potential (_x), leaf relative water content (RWC; % turgid weight), and xylem specific conductivity (K _S; kg s^–1 m^–1 MPa^–1) of sprouts were measured on two occasions during the dry season. In addition, K _S of seedlings (<1 year old) of one deciduous and one evergreen species was determined to allow comparison with sprouts. _x of deciduous species was significantly higher at the second sampling date and was accompanied by a significant increase in K _S and RWC, while the brevi-deciduous and evergreen species did not show any difference in _x. Seedlings of Terminalia crenulata (deciduous) and Ixora parviflora (evergreen) had significantly lower K _S compared to sprouts, while seedlings of all four deciduous species shed their leaves much earlier in the dry season than did conspecific sprouts. More favorable water relations of sprouts compared to seedlings during the peak of the dry season may explain the lower rates of die-back and mortality of sprouts observed in dry deciduous forests of India.

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This revised version was published online in May 2005 with corrections to Received-/Accepted-dates.