Photosynthesis,stomatal conductance and terpene emission response to water availability in dry and mesic Mediterranean forests

Key message

Warmer summer conditions result in increased terpene emissions except under severe drought, in which case they strongly decrease.

Abstract

Water stress results in a reduction of the metabolism of plants and in a reorganization of their use of resources geared to survival. In the Mediterranean region, periods of drought accompanied by high temperatures and high irradiance occur in summer. Plants have developed various mechanisms to survive in these conditions by resisting, tolerating or preventing stress. We used three typical Mediterranean tree species in Israel, Pinus halepensis L., Quercus calliprinos and Quercus ithaburensis Webb, as models for studying some of these adaptive mechanisms. We measured their photosynthetic rates (A), stomatal conductance (g _s), and terpene emission rates during spring and summer in a geophysical gradient from extremely dry to mesic from Yatir (south, arid) to Birya (north, moist) with intermediate conditions in Solelim. A and g _s of P. halepensis were threefold higher in Birya than in Yatir where they remained very low both seasons. Quercus species presented 2–3-fold higher A and g _s but with much more variability between seasons, especially for Q. ithaburensis with A and g _s that decreased 10–30-fold from spring to summer. Terpene emission rates for pine were not different regionally in spring but they were 5–8-fold higher in Birya than in Yatir in summer (P < 0.05). Higher emissions were also observed in Solelim for the drought resistant Q. ithaburensis (P < 0.001) but not for Q. calliprinos. α-Pinene followed by limonene and 3-carene were the dominant terpenes. Warmer summer conditions result in increased Terpene emission rates except under severe drought, in which case they strongly decrease.

     

Phenological response to climate change in China: a meta‐analysis

The change in the phenology of plants or animals reflects the response of living systems to climate change. Numerous studies have reported a consistent earlier spring phenophases in many parts of middle and high latitudes reflecting increasing temperatures with the exception of China. A systematic analysis of Chinese phenological response could complement the assessment of climate change impact for the whole Northern Hemisphere. Here, we analyze 1263 phenological time series (1960–2011, with 20+ years data) of 112 species extracted from 48 studies across 145 sites in China. Taxonomic groups include trees, shrubs, herbs, birds, amphibians and insects. Results demonstrate that 90.8% of the spring/summer phenophases time series show earlier trends and 69.0% of the autumn phenophases records show later trends. For spring/summer phenophases, the mean advance across all the taxonomic groups was 2.75 days decade^?1 ranging between 2.11 and 6.11 days decade^?1 for insects and amphibians, respectively. Herbs and amphibians show significantly stronger advancement than trees, shrubs and insect. The response of phenophases of different taxonomic groups in autumn is more complex: trees, shrubs, herbs and insects show a delay between 1.93 and 4.84 days decade^?1, while other groups reveal an advancement ranging from 1.10 to 2.11 days decade^?1. For woody plants (including trees and shrubs), the stronger shifts toward earlier spring/summer were detected from the data series starting from more recent decades (1980s–2000s). The geographic factors (latitude, longitude and altitude) could only explain 9% and 3% of the overall variance in spring/summer and autumn phenological trends, respectively. The rate of change in spring/summer phenophase of woody plants (1960s–2000s) generally matches measured local warming across 49 sites in China (R = ?0.33, P < 0.05).     

Decreasing water availability across the globe improves the effectiveness of protective ant–plant mutualisms: a meta‐analysis

Abiotic conditions can increase the costs of services and/or the benefits of rewards provided by mutualistic partners. Consequently, in some situations, the outcome of mutualisms can move from beneficial to detrimental for at least one partner. In the case of protective mutualisms between ant bodyguards and plants bearing extrafloral nectaries (EFNs), plants from arid environments face a trade‐off between EFN production and maintenance and water and carbon economy. This trade‐off may increase EFN costs and decrease their value as a defensive strategy to plants in such environments. Despite this, the presence of EFNs is an ubiquitous trait in plants from arid environments, suggesting that they provide greater benefits to plants in these environments to compensate for their higher costs. We used a meta‐analysis to investigate if such benefits do increase with decreasing water availability and the possible underlying causes (such as ant behaviour or ant diversity). As predicted, ant effect on EFN plants performance increased as mean annual precipitation decreased. We also found that the frequency of dominant ants on EFN plants increased in drier areas. Due to the more aggressive behaviour of dominant ants, we suggest that they represent an important factor shaping the adaptive value of EFNs to plants in arid environments.     

Body size and spatial scales in avian response to landscapes: a meta‐analysis

Response of species to their environment is dependent on the scales that individuals interact with landscapes. Several life‐history traits have been suggested to influence scales of response to landscapes, but little empirical work has addressed this issue, limiting our ability to predict the relevant scale(s) at which species respond to their environment. Body size is frequently hypothesized to be relevant for predicting the effects of landscape structure on species given correlations between body size and various measures of mobility or perceptual range, yet evidence of this relationship remains equivocal. We conducted a meta‐analysis of 22 studies to address the question of whether body size is related to the characteristic scale at which bird species respond to landscape structure. On the basis of correlation coefficients and linear mixed models, we show that body size is positively related to the characteristic scale of response to landscapes. The strength of this relationship is less than body size – dispersal allometries, suggesting that response to landscapes may be influenced, in part, by factors other than dispersal (e.g. territory size). However, the strength of the observed body size – scale relationship may have been affected by several factors, including limitations in the range of body sizes and landscape extents tested. Our findings suggest that life‐history traits mediate aspects of the scales at which species respond to the landscape and contribute to developing a more predictive framework for investigating scalar relationships in nature.     

冬小麦叶片气孔导度模型水分响应函数的参数化

植物气孔导度模型的水分响应函数用来模拟水分胁迫对气孔导度的影响过程, 是模拟缺水环境下植物与大气间水、碳交换过程的关键算法。水分响应函数包括空气湿度响应函数和土壤湿度(或植物水势)响应函数, 该研究基于田间实验观测, 分析了冬小麦(Triticum aestivum)叶片气孔导度对不同空气饱和差和不同土壤体积含水量或叶水势的响应规律。一个土壤水分梯度的田间处理在中国科学院禹城综合试验站实施, 不同水分胁迫下的冬小麦叶片气体交换过程和气孔导度以及其他的温湿度数据被观测, 同时观测了土壤含水量和叶水势。实验数据表明, 冬小麦叶片气孔导度对空气饱和差的响应呈现双曲线规律, 变化趋势显示大约1 kPa空气饱和差是一个有用的阈值, 在小于1 kPa时, 冬小麦气孔导度对空气饱和差变化反应敏感, 而大于1 kPa后则反应缓慢; 分析土壤体积含水量与中午叶片气孔导度的关系发现, 中午叶片气孔导度随土壤含水量增加大致呈现线性增加趋势, 但在平均土壤体积含水量大于大约25%以后, 气孔导度不再明显增加, 而是维持在较高导度值上下波动; 冬小麦中午叶片水势与相应的气孔导度之间, 随着叶水势的增加, 气孔导度呈现增加趋势。根据冬小麦气孔导度对空气湿度、土壤湿度和叶水势的响应规律, 研究分别采用双曲线和幂指数形式拟合了水汽响应函数, 用三段线性方程拟合了土壤湿度响应函数和植物水势响应函数, 得到的参数可以为模型模拟冬小麦的各类水、热、碳交换过程采用。     

The response of stomatal conductance to seasonal drought in tropical forests

Stomata regulate CO₂ uptake for photosynthesis and water loss through transpiration. The approaches used to represent stomatal conductance (g_s) in models vary. In particular, current understanding of drivers of the variation in a key parameter in those models, the slope parameter (i.e. a measure of intrinsic plant water‐use‐efficiency), is still limited, particularly in the tropics. Here we collected diurnal measurements of leaf gas exchange and leaf water potential (Ψ_leaf), and a suite of plant traits from the upper canopy of 15 tropical trees in two contrasting Panamanian forests throughout the dry season of the 2016 El Niño. The plant traits included wood density, leaf‐mass‐per‐area (LMA), leaf carboxylation capacity (V_c,max), leaf water content, the degree of isohydry, and predawn Ψ_leaf. We first investigated how the choice of four commonly used leaf‐level g_s models with and without the inclusion of Ψ_leaf as an additional predictor variable influence the ability to predict g_s, and then explored the abiotic (i.e. month, site‐month interaction) and biotic (i.e. tree‐species‐specific characteristics) drivers of slope parameter variation. Our results show that the inclusion of Ψ_leaf did not improve model performance and that the models that represent the response of g_s to vapor pressure deficit performed better than corresponding models that respond to relative humidity. Within each g_s model, we found large variation in the slope parameter, and this variation was attributable to the biotic driver, rather than abiotic drivers. We further investigated potential relationships between the slope parameter and the six available plant traits mentioned above, and found that only one trait, LMA, had a significant correlation with the slope parameter (R² = 0.66, n = 15), highlighting a potential path towards improved model parameterization. This study advances understanding of g_s dynamics over seasonal drought, and identifies a practical, trait‐based approach to improve modeling of carbon and water exchange in tropical forests.     

Oscillations in stomatal conductance and plant functioning associated with stomatal conductance: Observations and a model

Summary Measurements of transpiration, leaf water content, and flux of water in a cotton plant exhibiting sustained oscillations, in stomatal conductance are presented, and a model of the mechanism causing this behaviour is developed. The dynamic elements, of the model are capacitors—representing the change of water content with water potential in mesophyll, subsidiary and guard cells—interconnected by resistances representing flow paths in the plant. Increase of water potential in guard cells causes an increase in stomatal conductance. Increase of water potential in the subsidiary cells has the opposite effect and provides the positive feed-back which can cause stomatal conductance to oscillate. The oscillations are shown to have many of the characteristics of free-running oscillations in real plants. The behaviour of the model has been examined, using an analogue computer, with constraints and perturbations representing some of those which could be applied to real plants in physiological experiments. Aspects of behaviour which have been simulated are (a) opening and closing of stomata under the influence of changes in illumination, (b) transient responses due to step changes in potential transpiration, root permeability and potential of water surrounding the roots, (c) the influence of these factors on the occurrence and shape of spontaneous oscillations, and (d) modulation of sustained oscillations due to a circadian rhythm in the permeability of roots.     

Effects of macrophytes on lake‐water quality across latitudes: a meta‐analysis

Macrophytes are widely recognized for improving water quality and stabilizing the desirable clear‐water state in lakes. The positive effects of macrophytes on water quality have been noted to be weaker in the (sub)tropics compared to those of temperate regions. We conducted a global meta‐analysis using 47 studies that met our set criteria to assess the overall effects of macrophytes on water quality (measured by phytoplankton chlorophyll a concentration, total nitrogen concentration, total phosphorus concentration, Secchi depth and the trophic state index) and to investigate how these effects correlate with latitude using meta‐regressions. We also examined if the effects of macrophytes on lake‐water quality differ with growth form and study design in (sub)tropical and temperate areas by grouping the data and then comparing the effect sizes. We found that macrophytes significantly reduced phytoplankton chlorophyll a concentration, total nitrogen concentration, total phosphorus concentration, as well as the trophic state index, but they did not have a significant overall effect on Secchi depth. The effects of macrophytes on reducing phytoplankton chlorophyll a concentration, total nitrogen concentration and the trophic state index did not differ with latitude. However, the reduction of total phosphorus concentration was greater at lower latitudes. We showed that at lower latitudes, the positive effects of macrophytes on water quality are similar to or greater than those at higher latitudes, thus challenging the prevailing paradigm of macrophytes being less effective at enhancing lake‐water quality in the (sub)tropics. Furthermore, our data showed that the macrophyte effects vary by growth forms, and the growth forms that positively affect water quality differ between the (sub)tropical and temperate areas. We showed a lack of significant macrophyte effects in surveys within and outside macrophyte stands, suggesting difference in the sensitivities of study designs or possibly weaker effects of macrophytes in lakes compared to experimental settings.     

Microbial stress priming: a meta‐analysis

Microbes have to cope with complex and dynamic environments, making it likely that anticipatory responses provide fitness benefits. Mild, previous stressors can prepare microbes (stress priming) to further and potentially damaging stressors (triggering). We here quantitatively summarize the findings from over 250 trials of 34 studies including bacteria and fungi, demonstrating that priming to stress has a beneficial impact on microbial survival. In fact, survival of primed microbes was about 10‐fold higher compared with that in non‐primed microbes. Categorical moderators related to microbial taxonomy and the kind of stress applied as priming or as triggering revealed significant differences of priming effect size among 14 different microbial species, 6 stress categories and stressor combination. We found that priming by osmotic, physiological and temperature stress had the highest positive effect sizes on microbial response. Cross‐protection was evident for physiological, temperature and pH stresses. Microbes are better prepared against triggering by oxidative, temperature and osmotic stress. Our finding of an overall positive mean effect of priming regardless of the microbial system and particular stressor provides unprecedentedly strong evidence of the broad ecological significance of microbial stress priming. These results further suggest that stress priming may be an important factor in shaping microbial communities.     

Global response patterns of plant photosynthesis to nitrogen addition: A meta‐analysis

A mechanistic understanding of plant photosynthetic response is needed to reliably predict changes in terrestrial carbon (C) gain under conditions of chronically elevated atmospheric nitrogen (N) deposition. Here, using 2,683 observations from 240 journal articles, we conducted a global meta‐analysis to reveal effects of N addition on 14 photosynthesis‐related traits and affecting moderators. We found that across 320 terrestrial plant species, leaf N was enhanced comparably on mass basis (N_mass, +18.4%) and area basis (N_area, +14.3%), with no changes in specific leaf area or leaf mass per area. Total leaf area (TLA) was increased significantly, as indicated by the increases in total leaf biomass (+46.5%), leaf area per plant (+29.7%), and leaf area index (LAI, +24.4%). To a lesser extent than for TLA, N addition significantly enhanced leaf photosynthetic rate per area (A_area, +12.6%), stomatal conductance (g_s, +7.5%), and transpiration rate (E, +10.5%). The responses of A_area were positively related with that of g_s, with no changes in instantaneous water‐use efficiency and only slight increases in long‐term water‐use efficiency (+2.5%) inferred from ¹³C composition. The responses of traits depended on biological, experimental, and environmental moderators. As experimental duration and N load increased, the responses of LAI and A_area diminished while that of E increased significantly. The observed patterns of increases in both TLA and E indicate that N deposition will increase the amount of water used by plants. Taken together, N deposition will enhance gross photosynthetic C gain of the terrestrial plants while increasing their water loss to the atmosphere, but the effects on C gain might diminish over time and that on plant water use would be amplified if N deposition persists.     

A meta‐analysis of bird and mammal response to short‐rotation woody crops

Short‐rotation woody cropping (SRWC) refers to silvicultural systems designed to produce woody biomass using short harvest cycles (1–15 years), intensive silvicultural techniques, high‐yielding varieties, and often coppice regeneration. Recent emphasis on alternatives to fossil fuels has spurred interest in producing SRWC on privately owned and intensively managed forests of North America. We examined potential bird and small mammal response at the stand level to conversion of existing, intensively managed forests to SRWCs using meta‐analysis of existing studies. We found 257 effect sizes for birds (243 effect sizes) and mammals (14 effect sizes) from 8 studies involving Populus spp. plantations. Diversity and abundance of bird guilds were lower on short‐rotation plantations compared with reference woodlands, while abundance of individual bird species was more variable and not consistently higher or lower on SRWC plantations. Shrub‐associated birds were more abundant on SRWC plantations, but forest‐associated and cavity‐nesting birds were less abundant. Effects on birds appeared to decrease with age of the SRWC plantation, but plantation age was also confounded with variation in the type of reference forest used for comparison. Both guilds and species of mammals were less abundant on SRWC plantations. These conclusions are tentative because none of these studies directly compared SRWC plantations to intensively managed forests. Plantations of SRWCs could contribute to overall landscape diversity in forest‐dominated landscapes by providing shrubby habitat structure for nonforest species. However, extensive conversion of mature or intensively managed forests to SRWC would likely decrease overall diversity, especially if they replace habitat types of high conservation value.     

Stomatal and hydraulic conductance in growing sugarcane: stomatal adjustment to water transport capacity*

Abstract Stomatal conductance per unit leaf area in well-irrigated field- and greenhouse-grown sugarcane increased with leaf area up to 0.2 m² plant ¹, then declined so that maximum transpiration per plant tended to saturate rather than increase linearly with further increase in leaf area. Conductance to liquid water transport exhibited parallel changes with plant size. This coordiantion of vapour phase and liquid phase conductances resulted in a balance between water loss and water transport capacity, maintaining leaf water status remarkably constant over a wide range of plant size and growing conditions. The changes in stomatal conductance were not related to plant or leaf age. Partial defoliation caused rapid increases in stomatal conductance, to re-establish the original relationship with remaining leaf area. Similarly, pruning of roots caused rapid reductions in stomatal conductance, which maintained or improved leaf water status. These results suggest that sugarcane stomata adjusted to the ratio of total hydraulic conductance to total transpiring leaf area. This could be mediated by root metabolites in the transpiration stream, whose delivery per unit leaf area would be a function of the relative magnitudes of root system size, transpiration rate and leaf area.     

Differential coordination of stomatal conductance,mesophyll conductance,and leaf hydraulic conductance in response to changing light across species

Stomatal conductance (g_s) and mesophyll conductance (g_m) represent major constraints to photosynthetic rate (A), and these traits are expected to coordinate with leaf hydraulic conductance (K_leaf) across species, under both steady‐state and dynamic conditions. However, empirical information about their coordination is scarce. In this study, K_leaf, gas exchange, stomatal kinetics, and leaf anatomy in 10 species including ferns, gymnosperms, and angiosperms were investigated to elucidate the correlation of H₂O and CO₂ diffusion inside leaves under varying light conditions. Gas exchange, K_leaf, and anatomical traits varied widely across species. Under light‐saturated conditions, the A, g_s, g_m, and K_leaf were strongly correlated across species. However, the response patterns of A, g_s, g_m, and K_leaf to varying light intensities were highly species dependent. Moreover, stomatal opening upon light exposure of dark‐adapted leaves in the studied ferns and gymnosperms was generally faster than in the angiosperms; however, stomatal closing in light‐adapted leaves after darkening was faster in angiosperms. The present results show that there is a large variability in the coordination of leaf hydraulic and gas exchange parameters across terrestrial plant species, as well as in their responses to changing light.     

Estimating the sensitivity of stomatal conductance to photosynthesis: a review

A common approach for estimating fluxes of CO₂ and water in canopy models is to couple a model of photosynthesis (A_n) to a semi‐empirical model of stomatal conductance (g_s) such as the widely validated and utilized Ball–Berry (BB) model. This coupling provides an effective way of predicting transpiration at multiple scales. However, the designated value of the slope parameter (m) in the BB model impacts transpiration estimates. There is a lack of consensus regarding how m varies among species or plant functional types (PFTs) or in response to growth conditions. Literature values are highly variable, with inter‐species and intra‐species variations of >100%, and comparisons are made more difficult because of differences in collection techniques. This paper reviews the various methods used to estimate m and highlights how variations in measurement techniques or the data utilized can influence the resultant m. Additionally, this review summarizes the reported responses of m to [CO₂] and water stress, collates literature values by PFT and compiles nearly three decades of values into a useful compendium.     

The contribution of photosynthesis to the red light response of stomatal conductance

To determine the contribution of photosynthesis on stomatal conductance, we contrasted the stomatal red light response of wild-type tobacco (Nicotiana tabacum 'W38') with that of plants impaired in photosynthesis by antisense reductions in the content of either cytochrome b(6)f complex (anti-b/f plants) or Rubisco (anti-SSU plants). Both transgenic genotypes showed a lowered content of the antisense target proteins in guard cells as well as in the mesophyll. In the anti-b/f plants, CO(2) assimilation rates were proportional to leaf cytochrome b(6)f content, but there was little effect on stomatal conductance and the rate of stomatal opening. To compare the relationship between photosynthesis and stomatal conductance, wild-type plants and anti-SSU plants were grown at 30 and 300 micromol photon m(-2) s(-1) irradiance (low light and medium light [ML], respectively). Growth in ML increased CO(2) assimilation rates and stomatal conductance in both genotypes. Despite the significantly lower CO(2) assimilation rate in the anti-SSU plants, the differences in stomatal conductance between the genotypes were nonsignificant at either growth irradiance. Irrespective of plant genotype, stomatal density in the two leaf surfaces was 2-fold higher in ML-grown plants than in low-light-grown plants and conductance normalized to stomatal density was unaffected by growth irradiance. We conclude that the red light response of stomatal conductance is independent of the concurrent photosynthetic rate of the guard cells or of that of the underlying mesophyll. Furthermore, we suggest that the correlation of photosynthetic capacity and stomatal conductance observed under different light environments is caused by signals largely independent of photosynthesis.     

Sensitivity of coral calcification to ocean acidification: a meta‐analysis

To date, meta‐analyses of effects of acidification have focused on the overall strength of evidence for statistically significant responses; however, to anticipate likely consequences of ocean acidification, quantitative estimates of the magnitude of likely responses are also needed. Herein, we use random effects meta‐analysis to produce a systematically integrated measure of the distribution of magnitudes of the response of coral calcification to decreasing Ω_Arag. We also tested whether methodological and biological factors that have been hypothesized to drive variation in response magnitude explain a significant proportion of the among‐study variation. We found that the overall mean response of coral calcification is ~15% per unit decrease in Ω_Arag over the range 2 < Ω_Arag < 4. Among‐study variation is large (standard deviation of 8% per unit decrease in Ω_Arag). Neither differences in carbonate chemistry manipulation method, study duration, irradiance level, nor study species growth rate explained a significant proportion of the among‐study variation. However, studies employing buoyant weighting found significantly smaller decreases in calcification per unit Ω_Arag (~10%), compared with studies using the alkalinity anomaly technique (~25%). These differences may be due to the greater tendency for the former to integrate over light and dark calcification. If the existing body of experimental work is indeed representative of likely responses of corals in nature, our results imply that, under business as usual conditions, declines in coral calcification by end‐of‐century will be ~22%, on average, or ~15% if only studies integrating light and dark calcification are considered. These values are near the low end of published projections, but support the emerging view that variability due to local environmental conditions and species composition is likely to be substantial.