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1.  Leaf movements and their relationship with the lunisolar gravitational force 
Annals of Botany  2015;117(1):215.
PMCID: PMC4701157  PMID: 26453632
2.  Phototropic solar tracking in sunflower plants: an integrative perspective 
Annals of Botany  2015;117(1):1-8.
Background One of the best-known plant movements, phototropic solar tracking in sunflower (Helianthus annuus), has not yet been fully characterized. Two questions are still a matter of debate. (1) Is the adaptive significance solely an optimization of photosynthesis via the exposure of the leaves to the sun? (2) Is shade avoidance involved in this process? In this study, these concepts are discussed from a historical perspective and novel insights are provided.
Scope and Methods Results from the primary literature on heliotropic growth movements led to the conclusion that these responses cease before anthesis, so that the flowering heads point to the East. Based on observations on 10-week-old plants, the diurnal East–West oscillations of the upper fifth of the growing stem and leaves in relation to the position of the sun (inclusive of nocturnal re-orientation) were documented, and photon fluence rates on the leaf surfaces on clear, cloudy and rainy days were determined. In addition, the light–response curve of net CO2 assimilation was determined on the upper leaves of the same batch of plants, and evidence for the occurrence of shade-avoidance responses in growing sunflower plants is summarized.
Conclusions. Only elongating, vegetative sunflower shoots and the upper leaves perform phototropic solar tracking. Photon fluence response and CO2 assimilation measurements cast doubt on the ‘photosynthesis-optimization hypothesis’ as the sole explanation for the evolution of these plant movements. We suggest that the shade-avoidance response, which maximizes light-driven CO2 assimilation, plays a major role in solar tracking populations of competing sunflower plants, and an integrative scheme of these growth movements is provided.
PMCID: PMC4701145  PMID: 26420201
Phototropic solar tracking; photosynthesis; phototropism; plant movement; shade avoidance; solar tracking; sunflower; Helianthus annuus
3.  Genetic control of root growth: from genes to networks 
Annals of Botany  2015;117(1):9-24.
Background Roots are essential organs for higher plants. They provide the plant with nutrients and water, anchor the plant in the soil, and can serve as energy storage organs. One remarkable feature of roots is that they are able to adjust their growth to changing environments. This adjustment is possible through mechanisms that modulate a diverse set of root traits such as growth rate, diameter, growth direction and lateral root formation. The basis of these traits and their modulation are at the cellular level, where a multitude of genes and gene networks precisely regulate development in time and space and tune it to environmental conditions.
Scope This review first describes the root system and then presents fundamental work that has shed light on the basic regulatory principles of root growth and development. It then considers emerging complexities and how they have been addressed using systems-biology approaches, and then describes and argues for a systems-genetics approach. For reasons of simplicity and conciseness, this review is mostly limited to work from the model plant Arabidopsis thaliana, in which much of the research in root growth regulation at the molecular level has been conducted.
Conclusions While forward genetic approaches have identified key regulators and genetic pathways, systems-biology approaches have been successful in shedding light on complex biological processes, for instance molecular mechanisms involving the quantitative interaction of several molecular components, or the interaction of large numbers of genes. However, there are significant limitations in many of these methods for capturing dynamic processes, as well as relating these processes to genotypic and phenotypic variation. The emerging field of systems genetics promises to overcome some of these limitations by linking genotypes to complex phenotypic and molecular data using approaches from different fields, such as genetics, genomics, systems biology and phenomics.
PMCID: PMC4701154  PMID: 26558398
Root; root development; root growth; genetics; root patterning; systems biology; modelling; systems genetics; networks; Arabidopsis thaliana
4.  ContentSnapshots 
Annals of Botany  2015;117(1):i-iii.
PMCID: PMC4701158
5.  Plant Cuttings 
Annals of Botany  2015;117(1):iv-vi.
PMCID: PMC4701159
6.  Leaf mechanical resistance in plant trait databases: comparing the results of two common measurement methods 
Annals of Botany  2015;117(1):209-214.
Background and Aims The influence of leaf mechanical properties on local ecosystem processes, such as trophic transfer, decomposition and nutrient cycling, has resulted in a growing interest in including leaf mechanical resistance in large-scale databases of plant functional traits. ‘Specific work to shear’ and ‘force to tear’ are two properties commonly used to describe mechanical resistance (toughness or strength) of leaves. Two methodologies have been widely used to measure them across large datasets. This study aimed to assess correlations and standardization between the two methods, as measured by two widely used apparatuses, in order to inter-convert existing data in those global datasets.
Methods Specific work to shear (WSS) and force to tear (FT) were measured in leaves of 72 species from south-eastern Australia. The measurements were made including and excluding midribs. Relationships between the variables were tested by Spearman correlations and ordinary least square regressions.
Key Results A positive and significant correlation was found between the methods, but coefficients varied according to the inclusion or exclusion of the midrib in the measurements. Equations for prediction varied according to leaf venation pattern. A positive and significant (r = 0·90, P < 0·0001) correlation was also found between WSS values for fresh and rehydrated leaves, which is considered to be of practical relevance.
Conclusions In the context of broad-scale ecological hypotheses and used within the constraints recommended here, leaf mechanical resistance data obtained with both methodologies could be pooled together into a single coarser variable, using the equations provided in this paper. However, more detailed datasets of FT cannot be safely filled in with estimations based on WSS, or vice versa. In addition, WSS values of green leaves can be predicted with good accuracy from WSS of rehydrated leaves of the same species.
PMCID: PMC4717314  PMID: 26530215
Comparative plant ecology; force to tear; leaf biomechanics; leaf tensile strength; leaf toughness; leaf venation; specific work to shear; plant trait databases; work to shear
7.  Plants and climate change: complexities and surprises 
Annals of Botany  2015;116(6):849-864.
Background Anthropogenic climate change (ACC) will influence all aspects of plant biology over coming decades. Many changes in wild species have already been well-documented as a result of increased atmospheric CO2 concentrations, warming climate and changing precipitation regimes. A wealth of available data has allowed the use of meta-analyses to examine plant–climate interactions on more sophisticated levels than before. These analyses have revealed major differences in plant response among groups, e.g. with respect to functional traits, taxonomy, life-history and provenance. Interestingly, these meta-analyses have also exposed unexpected mismatches between theory, experimental, and observational studies.
Scope We reviewed the literature on species’ responses to ACC, finding ∼42 % of 4000 species studied globally are plants (primarily terrestrial). We review impacts on phenology, distributions, ecophysiology, regeneration biology, plant–plant and plant–herbivore interactions, and the roles of plasticity and evolution. We focused on apparent deviations from expectation, and highlighted cases where more sophisticated analyses revealed that unexpected changes were, in fact, responses to ACC.
Conclusions We found that conventionally expected responses are generally well-understood, and that it is the aberrant responses that are now yielding greater insight into current and possible future impacts of ACC. We argue that inconclusive, unexpected, or counter-intuitive results should be embraced in order to understand apparent disconnects between theory, prediction, and observation. We highlight prime examples from the collection of papers in this Special Issue, as well as general literature. We found use of plant functional groupings/traits had mixed success, but that some underutilized approaches, such as Grime's C/S/R strategies, when incorporated, have improved understanding of observed responses. Despite inherent difficulties, we highlight the need for ecologists to conduct community-level experiments in systems that replicate multiple aspects of ACC. Specifically, we call for development of coordinating experiments across networks of field sites, both natural and man-made.
PMCID: PMC4640131  PMID: 26555281
Climate change; global change; phenology; distributions; range shifts; invasive species; assisted colonization; elevated CO2; plant functional groups; plant functional traits; plasticity; evolution.
8.  Phosphorus application and elevated CO2 enhance drought tolerance in field pea grown in a phosphorus-deficient vertisol 
Annals of Botany  2014;116(6):975-985.
Background and Aims Benefits to crop productivity arising from increasing CO2 fertilization may be offset by detrimental effects of global climate change, such as an increasing frequency of drought. Phosphorus (P) nutrition plays an important role in crop responses to water stress, but how elevated CO2 (eCO2) and P nutrition interact, especially in legumes, is unclear. This study aimed to elucidate whether P supply improves plant drought tolerance under eCO2.
Methods A soil-column experiment was conducted in a free air CO2 enrichment (SoilFACE) system. Field pea (Pisum sativum) was grown in a P-deficient vertisol, supplied with 15 mg P kg−1 (deficient) or 60 mg P kg−1 (adequate for crop growth) and exposed to ambient CO2 (aCO2; 380–400 ppm) or eCO2 (550–580 ppm). Drought treatments commenced at flowering. Measurements were taken of soil and leaf water content, photosynthesis, stomatal conductance, total soluble sugars and inorganic P content (Pi).
Key Results Water-use efficiency was greatest under eCO2 when the plants were supplied with adequate P compared with other treatments irrespective of drought treatment. Elevated CO2 decreased stomatal conductance and transpiration rate, and increased the concentration of soluble sugars and relative water contents in leaves. Adequate P supply increased concentrations of soluble sugars and Pi in drought-stressed plants. Adequate P supply but not eCO2 increased root length distribution in deeper soil layers.
Conclusions Phosphorus application and eCO2 interactively enhanced periodic drought tolerance in field pea as a result of decreased stomatal conductance, deeper rooting and high Pi availability for carbon assimilation in leaves.
PMCID: PMC4640114  PMID: 25429008
Climate change; crop nutrition; drought tolerance; free air CO2 enrichment; FACE; P nutrition; pea; Pisum sativum; root length distribution; stomatal conductance; water-use efficiency
9.  Plant communities on infertile soils are less sensitive to climate change 
Annals of Botany  2014;116(6):1017-1022.
Background and Aims Much evidence suggests that plant communities on infertile soils are relatively insensitive to increased water deficit caused by increasing temperature and/or decreasing precipitation. However, a multi-decadal study of community change in the western USA does not support this conclusion. This paper tests explanations related to macroclimatic differences, overstorey effects on microclimate, variation in soil texture and plant functional traits.
Methods A re-analysis was undertaken of the changes in the multi-decadal study, which concerned forest understorey communities on infertile (serpentine) and fertile soils in an aridifying climate (southern Oregan) from 1949–1951 to 2007–2008. Macroclimatic variables, overstorey cover and soil texture were used as new covariates. As an alternative measure of climate-related change, the community mean value of specific leaf area was used, a functional trait measuring drought tolerance. We investigated whether these revised analyses supported the prediction of lesser sensitivity to climate change in understorey communities on infertile serpentine soils.
Key Results Overstorey cover, but not macroclimate or soil texture, was a significant covariate of community change over time. It strongly buffered understorey temperatures, was correlated with less change and averaged >50 % lower on serpentine soils, thereby counteracting the lower climate sensitivity of understorey herbs on these soils. Community mean specific leaf area showed the predicted pattern of less change over time in serpentine than non-serpentine communities.
Conclusions Based on the current balance of evidence, plant communities on infertile serpentine soils are less sensitive to changes in the climatic water balance than communities on more fertile soils. However, this advantage may in some cases be lessened by their sparser overstorey cover.
PMCID: PMC4640116  PMID: 25452247
Plant community change; climate change; climate resistance; climate resilience; soil fertility; stress tolerance; plant functional traits; serpentine soil; specific leaf area; biogeographical affinity; topographic affinity; Klamath–Siskiyou
10.  Substantial variation in leaf senescence times among 1360 temperate woody plant species: implications for phenology and ecosystem processes 
Annals of Botany  2015;116(6):865-873.
Background and Aims Autumn leaf senescence marks the end of the growing season in temperate ecosystems. Its timing influences a number of ecosystem processes, including carbon, water and nutrient cycling. Climate change is altering leaf senescence phenology and, as those changes continue, it will affect individual woody plants, species and ecosystems. In contrast to spring leaf out times, however, leaf senescence times remain relatively understudied. Variation in the phenology of leaf senescence among species and locations is still poorly understood.
Methods Leaf senescence phenology of 1360 deciduous plant species at six temperate botanical gardens in Asia, North America and Europe was recorded in 2012 and 2013. This large data set was used to explore ecological and phylogenetic factors associated with variation in leaf senescence.
Key Results Leaf senescence dates among species varied by 3 months on average across the six locations. Plant species tended to undergo leaf senescence in the same order in the autumns of both years at each location, but the order of senescence was only weakly correlated across sites. Leaf senescence times were not related to spring leaf out times, were not evolutionarily conserved and were only minimally influenced by growth habit, wood anatomy and percentage colour change or leaf drop. These weak patterns of leaf senescence timing contrast with much stronger leaf out patterns from a previous study.
Conclusions The results suggest that, in contrast to the broader temperature effects that determine leaf out times, leaf senescence times are probably determined by a larger or different suite of local environmental effects, including temperature, soil moisture, frost and wind. Determining the importance of these factors for a wide range of species represents the next challenge for understanding how climate change is affecting the end of the growing season and associated ecosystem processes.
PMCID: PMC4640117  PMID: 25808654
Leaf senescence; phenology; growing season; phylogeny; botanical gardens; climate change; deciduous woody plants; trees; shrubs; vines
11.  From observations to experiments in phenology research: investigating climate change impacts on trees and shrubs using dormant twigs 
Annals of Botany  2015;116(6):889-897.
Background and Aims Climate change is advancing the leaf-out times of many plant species and mostly extending the growing season in temperate ecosystems. Laboratory experiments using twig cuttings from woody plant species present an affordable, easily replicated approach to investigate the relative importance of factors such as winter chilling, photoperiod, spring warming and frost tolerance on the leafing-out times of plant communities. This Viewpoint article demonstrates how the results of these experiments deepen our understanding beyond what is possible via analyses of remote sensing and field observation data, and can be used to improve climate change forecasts of shifts in phenology, ecosystem processes and ecological interactions.
Scope The twig method involves cutting dormant twigs from trees, shrubs and vines on a single date or at intervals over the course of the winter and early spring, placing them in containers of water in controlled environments, and regularly recording leaf-out, flowering or other phenomena. Prior to or following leaf-out or flowering, twigs may be assigned to treatment groups for experiments involving temperature, photoperiod, frost, humidity and more. Recent studies using these methods have shown that winter chilling requirements and spring warming strongly affect leaf-out and flowering times of temperate trees and shrubs, whereas photoperiod requirements are less important than previously thought for most species. Invasive plant species have weaker winter chilling requirements than native species in temperate ecosystems, and species that leaf-out early in the season have greater frost tolerance than later leafing species.
Conclusions This methodology could be extended to investigate additional drivers of leaf-out phenology, leaf senescence in the autumn, and other phenomena, and could be a useful tool for education and outreach. Additional ecosystems, such as boreal, southern hemisphere and sub-tropical forests, could also be investigated using dormant twigs to determine the drivers of leaf-out times and how these ecosystems will be affected by climate change.
PMCID: PMC4640118  PMID: 25851135
Dormant twigs; woody plants; phenology; leaf-out; flowering time; phenology; climate change; winter chilling; photoperiod; humidity; frost tolerance; trees; shrubs; invasive species
12.  What functional strategies drive drought survival and recovery of perennial species from upland grassland? 
Annals of Botany  2015;116(6):1001-1015.
Background and Aims Extreme climatic events such as severe droughts are expected to increase with climate change and to limit grassland perennity. The present study aimed to characterize the adaptive responses by which temperate herbaceous grassland species resist, survive and recover from a severe drought and to explore the relationships between plant resource use and drought resistance strategies.
Methods Monocultures of six native perennial species from upland grasslands and one Mediterranean drought-resistant cultivar were compared under semi-controlled and non-limiting rooting depth conditions. Above- and below-ground traits were measured under irrigation in spring and during drought in summer (50 d of withholding water) in order to characterize resource use and drought resistance strategies. Plants were then rehydrated and assessed for survival (after 15 d) and recovery (after 1 year).
Key Results Dehydration avoidance through water uptake was associated with species that had deep roots (>1·2 m) and high root mass (>4 kg m−3). Cell membrane stability ensuring dehydration tolerance of roots and meristems was positively correlated with fructan content and negatively correlated with sucrose content. Species that survived and recovered best combined high resource acquisition in spring (leaf elongation rate >9 mm d−1 and rooting depth >1·2 m) with both high dehydration avoidance and tolerance strategies.
Conclusions Most of the native forage species, dominant in upland grassland, were able to survive and recover from extreme drought, but with various time lags. Overall the results suggest that the wide range of interspecific functional strategies for coping with drought may enhance the resilience of upland grassland plant communities under extreme drought events.
PMCID: PMC4640119  PMID: 25851134
Dehydration avoidance; dehydration tolerance; drought survival; forbs; fructans; functional traits; grasses; membrane stability; resilience index; root system; sucrose; upland grassland
13.  Artificial asymmetric warming reduces nectar yield in a Tibetan alpine species of Asteraceae 
Annals of Botany  2015;116(6):899-906.
Background and Aims Asymmetric warming is one of the distinguishing features of global climate change, in which winter and night-time temperatures are predicted to increase more than summer and diurnal temperatures. Winter warming weakens vernalization and hence decreases the potential to flower for some perennial herbs, and night warming can reduce carbohydrate concentrations in storage organs. This study therefore hypothesized that asymmetric warming should act to reduce flower number and nectar production per flower in a perennial herb, Saussurea nigrescens, a key nectar plant for pollinators in Tibetan alpine meadows.
Methods A long-term (6 years) warming experiment was conducted using open-top chambers placed in a natural meadow and manipulated to achieve asymmetric increases in temperature, as follows: a mean annual increase of 0·7 and 2·7 °C during the growing and non-growing seasons, respectively, combined with an increase of 1·6 and 2·8 °C in the daytime and night-time, respectively, from June to August. Measurements were taken of nectar volume and concentration (sucrose content), and also of leaf non-structural carbohydrate content and plant morphology.
Key Results Six years of experimental warming resulted in reductions in nectar volume per floret (64·7 % of control), floret number per capitulum (8·7 %) and capitulum number per plant (32·5 %), whereas nectar concentration remained unchanged. Depletion of leaf non-structural carbohydrates was significantly higher in the warmed than in the ambient condition. Overall plant density was also reduced by warming, which, when combined with reductions in flower development and nectar volumes, led to a reduction of ∼90 % in nectar production per unit area.
Conclusions The negative effect of asymmetric warming on nectar yields in S. nigrescens may be explained by a concomitant depletion of leaf non-structural carbohydrates. The results thus highlight a novel aspect of how climate change might affect plant–pollinator interactions and plant reproduction via induction of allocation shifts for plants growing in communities subject to asymmetric warming.
PMCID: PMC4640121  PMID: 25921787
Global climate change; asymmetric warming; nectar rewards; nectar yield; alpine meadow; Saussurea nigrescens; Asteraceae; plant–pollinator interactions; non-structural carbohydrates
14.  Does long-term cultivation of saplings under elevated CO2 concentration influence their photosynthetic response to temperature? 
Annals of Botany  2015;116(6):929-939.
Background and Aims Plants growing under elevated atmospheric CO2 concentrations often have reduced stomatal conductance and subsequently increased leaf temperature. This study therefore tested the hypothesis that under long-term elevated CO2 the temperature optima of photosynthetic processes will shift towards higher temperatures and the thermostability of the photosynthetic apparatus will increase.
Methods The hypothesis was tested for saplings of broadleaved Fagus sylvatica and coniferous Picea abies exposed for 4–5 years to either ambient (AC; 385 µmol mol−1) or elevated (EC; 700 µmol mol−1) CO2 concentrations. Temperature response curves of photosynthetic processes were determined by gas-exchange and chlorophyll fluorescence techniques.
Key Results Initial assumptions of reduced light-saturated stomatal conductance and increased leaf temperatures for EC plants were confirmed. Temperature response curves revealed stimulation of light-saturated rates of CO2 assimilation (Amax) and a decline in photorespiration (RL) as a result of EC within a wide temperature range. However, these effects were negligible or reduced at low and high temperatures. Higher temperature optima (Topt) of Amax, Rubisco carboxylation rates (VCmax) and RL were found for EC saplings compared with AC saplings. However, the shifts in Topt of Amax were instantaneous, and disappeared when measured at identical CO2 concentrations. Higher values of Topt at elevated CO2 were attributed particularly to reduced photorespiration and prevailing limitation of photosynthesis by ribulose-1,5-bisphosphate (RuBP) regeneration. Temperature response curves of fluorescence parameters suggested a negligible effect of EC on enhancement of thermostability of photosystem II photochemistry.
Conclusions Elevated CO2 instantaneously increases temperature optima of Amax due to reduced photorespiration and limitation of photosynthesis by RuBP regeneration. However, this increase disappears when plants are exposed to identical CO2 concentrations. In addition, increased heat-stress tolerance of primary photochemistry in plants grown at elevated CO2 is unlikely. The hypothesis that long-term cultivation at elevated CO2 leads to acclimation of photosynthesis to higher temperatures is therefore rejected. Nevertheless, incorporating acclimation mechanisms into models simulating carbon flux between the atmosphere and vegetation is necessary.
PMCID: PMC4640122  PMID: 25851132
Climate change; CO2 assimilation; elevated CO2 acclimation; European beech; Fagus sylvatica; Norway spruce; photorespiration; photosystem II photochemistry; Picea abies; Rubisco carboxylation; thermotolerance
15.  A climate change context for the decline of a foundation tree species in south-western Australia: insights from phylogeography and species distribution modelling 
Annals of Botany  2015;116(6):941-952.
Background and Aims A worldwide increase in tree decline and mortality has been linked to climate change and, where these represent foundation species, this can have important implications for ecosystem functions. This study tests a combined approach of phylogeographic analysis and species distribution modelling to provide a climate change context for an observed decline in crown health and an increase in mortality in Eucalyptus wandoo, an endemic tree of south-western Australia.
Methods Phylogeographic analyses were undertaken using restriction fragment length polymorphism analysis of chloroplast DNA in 26 populations across the species distribution. Parsimony analysis of haplotype relationships was conducted, a haplotype network was prepared, and haplotype and nucleotide diversity were calculated. Species distribution modelling was undertaken using Maxent models based on extant species occurrences and projected to climate models of the last glacial maximum (LGM).
Key Results A structured pattern of diversity was identified, with the presence of two groups that followed a climatic gradient from mesic to semi-arid regions. Most populations were represented by a single haplotype, but many haplotypes were shared among populations, with some having widespread distributions. A putative refugial area with high haplotype diversity was identified at the centre of the species distribution. Species distribution modelling showed high climatic suitability at the LGM and high climatic stability in the central region where higher genetic diversity was found, and low suitability elsewhere, consistent with a pattern of range contraction.
Conclusions Combination of phylogeography and paleo-distribution modelling can provide an evolutionary context for climate-driven tree decline, as both can be used to cross-validate evidence for refugia and contraction under harsh climatic conditions. This approach identified a central refugial area in the test species E. wandoo, with more recent expansion into peripheral areas from where it had contracted at the LGM. This signature of contraction from lower rainfall areas is consistent with current observations of decline on the semi-arid margin of the range, and indicates low capacity to tolerate forecast climatic change. Identification of a paleo-historical context for current tree decline enables conservation interventions to focus on maintaining genetic diversity, which provides the evolutionary potential for adaptation to climate change.
PMCID: PMC4640123  PMID: 25851142
Climate change; Eucalyptus wandoo; Myrtaceae; evolution; forest decline; haplotypes; last glacial maximum; LGM; phylogeography; refugia; species distribution modelling; tree decline.
16.  Changes in autumn senescence in northern hemisphere deciduous trees: a meta-analysis of autumn phenology studies 
Annals of Botany  2015;116(6):875-888.
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.
PMCID: PMC4640124  PMID: 25968905
Autumn phenology; climate change; growing season; leaf senescence; temperature; deciduous tree; woody plants
17.  The impact of elevated carbon dioxide on the phosphorus nutrition of plants: a review 
Annals of Botany  2015;116(6):987-999.
Background Increasing attention is being focused on the influence of rapid increases in atmospheric CO2 concentration on nutrient cycling in ecosystems. An understanding of how elevated CO2 affects plant utilization and acquisition of phosphorus (P) will be critical for P management to maintain ecosystem sustainability in P-deficient regions.
Scope This review focuses on the impact of elevated CO2 on plant P demand, utilization in plants and P acquisition from soil. Several knowledge gaps on elevated CO2-P associations are highlighted.
Conclusions Significant increases in P demand by plants are likely to happen under elevated CO2 due to the stimulation of photosynthesis, and subsequent growth responses. Elevated CO2 alters P acquisition through changes in root morphology and increases in rooting depth. Moreover, the quantity and composition of root exudates are likely to change under elevated CO2, due to the changes in carbon fluxes along the glycolytic pathway and the tricarboxylic acid cycle. As a consequence, these root exudates may lead to P mobilization by the chelation of P from sparingly soluble P complexes, by the alteration of the biochemical environment and by changes to microbial activity in the rhizosphere. Future research on chemical, molecular, microbiological and physiological aspects is needed to improve understanding of how elevated CO2 might affect the use and acquisition of P by plants.
PMCID: PMC4640125  PMID: 26113632
Elevated CO2; climate change; plant nutrition; phosphorous uptake; P transformation; P-use efficiency; root morphology; root exudates; microbial community.
18.  Climate warming could increase recruitment success in glacier foreland plants 
Annals of Botany  2015;116(6):907-916.
Background and Aims Glacier foreland plants are highly threatened by global warming. Regeneration from seeds on deglaciated terrain will be crucial for successful migration and survival of these species, and hence a better understanding of the impacts of climate change on seedling recruitment is urgently needed to predict future plant persistence in these environments. This study presents the first field evidence of the impact of climate change on recruitment success of glacier foreland plants.
Methods Seeds of eight foreland species were sown on a foreland site at 2500 m a.s.l., and at a site 400 m lower in altitude to simulate a 2·7 °C increase in mean annual temperature. Soil from the site of origin was used to reproduce the natural germination substrate. Recruitment success, temperature and water potential were monitored for 2 years. The response of seed germination to warming was further investigated in the laboratory.
Key Results At the glacier foreland site, seedling emergence was low (0 to approx. 40 %) and occurred in summer in all species after seeds had experienced autumn and winter seasons. However, at the warmer site there was a shift from summer to autumn emergence in two species and a significant increase of summer emergence (13–35 % higher) in all species except two. Survival and establishment was possible for 60–75 % of autumn-emerged seedlings and was generally greater under warmer conditions. Early snowmelt in spring caused the main ecological factors enhancing the recruitment success.
Conclusions The results suggest that warming will influence the recruitment of glacier foreland species primarily via the extension of the snow-free period in spring, which increases seedling establishment and results in a greater resistance to summer drought and winter extremes. The changes in recruitment success observed here imply that range shifts or changes in abundance are possible in a future warmer climate, but overall success may be dependent on interactions with shifts in other components of the plant community.
PMCID: PMC4640126  PMID: 26133689
Adaptation; alpine plants; climate change; glacier foreland plants; global warming; seed germination; seedling recruitment; seedling survival
19.  Biotic context and soil properties modulate native plant responses to enhanced rainfall 
Annals of Botany  2015;116(6):963-973.
Background and Aims The environmental and biotic context within which plants grow have a great potential to modify responses to climatic changes, yet few studies have addressed both the direct effects of climate and the modulating roles played by variation in the biotic (e.g. competitors) and abiotic (e.g. soils) environment.
Methods In a grassland with highly heterogeneous soils and community composition, small seedlings of two native plants, Lasthenia californica and Calycadenia pauciflora, were transplanted into factorially watered and fertilized plots. Measurements were made to test how the effect of climatic variability (mimicked by the watering treatment) on the survival, growth and seed production of these species was modulated by above-ground competition and by edaphic variables.
Key Results Increased competition outweighed the direct positive impacts of enhanced rainfall on most fitness measures for both species, resulting in no net effect of enhanced rainfall. Both species benefitted from enhanced rainfall when the absence of competitors was accompanied by high soil water retention capacity. Fertilization did not amplify the watering effects; rather, plants benefitted from enhanced rainfall or competitor removal only in ambient nutrient conditions with high soil water retention capacity.
Conclusions The findings show that the direct effects of climatic variability on plant fitness may be reversed or neutralized by competition and, in addition, may be strongly modulated by soil variation. Specifically, coarse soil texture was identified as a factor that may limit plant responsiveness to altered water availability. These results highlight the importance of considering the abiotic as well as biotic context when making future climate change forecasts.
PMCID: PMC4640127  PMID: 26159934
Biotic context; California annual natives; Calycadenia pauciflora; climate change; competition; direct and indirect effects; enhanced rainfall; floral herbivory; grassland; Lasthenia californica; multiple global changes; plant–climate interactions; soil properties
20.  Know your limits? Climate extremes impact the range of Scots pine in unexpected places 
Annals of Botany  2015;116(6):917-927.
Background and Aims Although extreme climatic events such as drought are known to modify forest dynamics by triggering tree dieback, the impact of extreme cold events, especially at the low-latitude margin (‘rear edge’) of species distributional ranges, has received little attention. The aim of this study was to examine the impact of one such extreme cold event on a population of Scots pine (Pinus sylvestris) along the species’ European southern rear-edge range limit and to determine how such events can be incorporated into species distribution models (SDMs).
Methods A combination of dendrochronology and field observation was used to quantify how an extreme cold event in 2001 in eastern Spain affected growth, needle loss and mortality of Scots pine. Long-term European climatic data sets were used to contextualize the severity of the 2001 event, and an SDM for Scots pine in Europe was used to predict climatic range limits.
Key Results The 2001 winter reached record minimum temperatures (equivalent to the maximum European-wide diurnal ranges) and, for trees already stressed by a preceding dry summer and autumn, this caused dieback and large-scale mortality. Needle loss and mortality were particularly evident in south-facing sites, where post-event recovery was greatly reduced. The SDM predicted European Scots pine distribution mainly on the basis of responses to maximum and minimum monthly temperatures, but in comparison with this the observed effects of the 2001 cold event at the southerly edge of the range limit were unforeseen.
Conclusions The results suggest that in order to better forecast how anthropogenic climate change might affect future forest distributions, distribution modelling techniques such as SDMs must incorporate climatic extremes. For Scots pine, this study shows that the effects of cold extremes should be included across the entire distribution margin, including the southern ‘rear edge’, in order to avoid biased predictions based solely on warmer climatic scenarios.
PMCID: PMC4640128  PMID: 26292992
Dendrochronology; climate change; drought; extreme climate; freeze event; Pinus sylvestris; range-shifts; rear edge; Scots pine; species distribution model
21.  Lower plasticity exhibited by high- versus mid-elevation species in their phenological responses to manipulated temperature and drought 
Annals of Botany  2015;116(6):953-962.
Background and Aims Recent global changes, particularly warming and drought, have had worldwide repercussions on the timing of flowering events for many plant species. Phenological shifts have also been reported in alpine environments, where short growing seasons and low temperatures make reproduction particularly challenging, requiring fine-tuning to environmental cues. However, it remains unclear if species from such habitats, with their specific adaptations, harbour the same potential for phenological plasticity as species from less demanding habitats.
Methods Fourteen congeneric species pairs originating from mid and high elevation were reciprocally transplanted to common gardens at 1050 and 2000 m a.s.l. that mimic prospective climates and natural field conditions. A drought treatment was implemented to assess the combined effects of temperature and precipitation changes on the onset and duration of reproductive phenophases. A phenotypic plasticity index was calculated to evaluate if mid- and high-elevation species harbour the same potential for plasticity in reproductive phenology.
Key Results Transplantations resulted in considerable shifts in reproductive phenology, with highly advanced initiation and shortened phenophases at the lower (and warmer) site for both mid- and high-elevation species. Drought stress amplified these responses and induced even further advances and shortening of phenophases, a response consistent with an ‘escape strategy’. The observed phenological shifts were generally smaller in number of days for high-elevation species and resulted in a smaller phenotypic plasticity index, relative to their mid-elevation congeners.
Conclusions While mid- and high-elevation species seem to adequately shift their reproductive phenology to track ongoing climate changes, high-elevation species were less capable of doing so and appeared more genetically constrained to their specific adaptations to an extreme environment (i.e. a short, cold growing season).
PMCID: PMC4640129  PMID: 26424784
Climate change; flowering phenology; phenotypic plasticity; global warming; drought; common garden; mid-elevation and high-elevation species; Swiss Alps
22.  ContentSnapshots 
Annals of Botany  2015;116(6):i-iii.
PMCID: PMC4640130
25.  A traits-based test of the home-field advantage in mixed-species tree litter decomposition 
Annals of Botany  2015;116(5):781-788.
Background and Aims Litter often decomposes faster in its environment of origin (at ‘home’) than in a foreign environment (‘away’), which has become known as the home-field advantage (HFA). However, many studies have highlighted the conditional nature of the HFA, suggesting that current understanding of this phenomenon is not yet sufficient to generalize across systems.
Methods The HFA hypothesis was tested for mono-specific and mixed-species litter using a tree-based experiment that manipulated the functional identity and diversity of the host tree community. Litter types of varying quality were transplanted between several host tree communities and decomposition rates were measured using litterbags. Since the decomposer community should respond to traits of the litter input and not their taxonomic identity, a traits-based index of litter–tree similarity was developed.
Key Results Mono-specific litter exhibited HFA, but when the same litter was decomposed in mixture, this trend was not observed. Mixed-species litter decomposed on average no faster or slower than monoculture litter and exhibited both positive and negative species interactions. These non-additive interactions of decomposition rates in mixture were influenced by the degree of similarity between litter and tree traits. Both synergistic and antagonistic interactions decreased in magnitude with increasing litter–tree similarity such that mixture rates were predictable from monocultures.
Conclusions The HFA occurred more strongly for mono-specific litter than for the litter types mixed together because interactions between species may have masked this effect. However, when expressed as a function of trait similarity between litters and tree communities, the HFA was not detected.
PMCID: PMC4590322  PMID: 26162398
Home-field advantage; HFA; tree litter decomposition; mixed-species litter; biodiversity; plant functional traits

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