Optimal stomatal theory predicts CO2 responses of stomatal conductance in both gymnosperm and angiosperm trees.

Optimal stomatal theory predicts that stomata operate to maximise photosynthesis (Anet ) and minimise transpirational water loss to achieve optimal intrinsic water-use efficiency (iWUE). We tested whether this theory can predict stomatal responses to elevated atmospheric CO2 (eCO2 ), and whether it can capture differences in responsiveness among woody plant functional types (PFTs). We conducted a meta-analysis of tree studies of the effect of eCO2 on iWUE and its components Anet and stomatal conductance (gs ). We compared three PFTs, using the unified stomatal optimisation (USO) model to account for confounding effects of leaf-air vapour pressure difference (D). We expected smaller gs , but greater Anet , responses to eCO2 in gymnosperms compared with angiosperm PFTs. We found that iWUE increased in proportion to increasing eCO2 in all PFTs, and that increases in Anet had stronger effects than reductions in gs . The USO model correctly captured stomatal behaviour with eCO2 across most datasets. The chief difference among PFTs was a lower stomatal slope parameter (g1 ) for the gymnosperm, compared with angiosperm, species. Land surface models can use the USO model to describe stomatal behaviour under changing atmospheric CO2 conditions.

When things get MESI: The Manipulation Experiments Synthesis Initiative-A coordinated effort to synthesize terrestrial global change experiments.

Responses of the terrestrial biosphere to rapidly changing environmental conditions are a major source of uncertainty in climate projections. In an effort to reduce this uncertainty, a wide range of global change experiments have been conducted that mimic future conditions in terrestrial ecosystems, manipulating CO2 , temperature, and nutrient and water availability. Syntheses of results across experiments provide a more general sense of ecosystem responses to global change, and help to discern the influence of background conditions such as climate and vegetation type in determining global change responses. Several independent syntheses of published data have yielded distinct databases for specific objectives. Such parallel, uncoordinated initiatives carry the risk of producing redundant data collection efforts and have led to contrasting outcomes without clarifying the underlying reason for divergence. These problems could be avoided by creating a publicly available, updatable, curated database. Here, we report on a global effort to collect and curate 57,089 treatment responses across 3644 manipulation experiments at 1145 sites, simulating elevated CO2 , warming, nutrient addition, and precipitation changes. In the resulting Manipulation Experiments Synthesis Initiative (MESI) database, effects of experimental global change drivers on carbon and nutrient cycles are included, as well as ancillary data such as background climate, vegetation type, treatment magnitude, duration, and, unique to our database, measured soil properties. Our analysis of the database indicates that most experiments are short term (one or few growing seasons), conducted in the USA, Europe, or China, and that the most abundantly reported variable is aboveground biomass. We provide the most comprehensive multifactor global change database to date, enabling the research community to tackle open research questions, vital to global policymaking. The MESI database, freely accessible at doi.org/10.5281/zenodo.7153253, opens new avenues for model evaluation and synthesis-based understanding of how global change affects terrestrial biomes. We welcome contributions to the database on GitHub.

Plant growth: the What, the How, and the Why.

Growth is a widely used term in plant science and ecology, but it can have different meanings depending on the context and the spatiotemporal scale of analysis. At the meristem level, growth is associated with the production of cells and initiation of new organs. At the organ or plant scale and over short time periods, growth is often used synonymously with tissue expansion, while over longer time periods the increase in biomass is a common metric. At even larger temporal and spatial scales, growth is mostly described as net primary production. Here, we first address the question 'what is growth?'. We propose a general framework to distinguish between the different facets of growth, and the corresponding physiological processes, environmental drivers and mathematical formalisms. Based on these different definitions, we then review how plant growth can be measured and analysed at different organisational, spatial and temporal scales. We conclude by discussing why gaining a better understanding of the different facets of plant growth is essential to disentangle genetic and environmental effects on the phenotype, and to uncover the causalities around source or sink limitations of plant growth.

Integrating the evidence for a terrestrial carbon sink caused by increasing atmospheric CO2.

Atmospheric carbon dioxide concentration ([CO2 ]) is increasing, which increases leaf-scale photosynthesis and intrinsic water-use efficiency. These direct responses have the potential to increase plant growth, vegetation biomass, and soil organic matter; transferring carbon from the atmosphere into terrestrial ecosystems (a carbon sink). A substantial global terrestrial carbon sink would slow the rate of [CO2 ] increase and thus climate change. However, ecosystem CO2 responses are complex or confounded by concurrent changes in multiple agents of global change and evidence for a [CO2 ]-driven terrestrial carbon sink can appear contradictory. Here we synthesize theory and broad, multidisciplinary evidence for the effects of increasing [CO2 ] (iCO2 ) on the global terrestrial carbon sink. Evidence suggests a substantial increase in global photosynthesis since pre-industrial times. Established theory, supported by experiments, indicates that iCO2 is likely responsible for about half of the increase. Global carbon budgeting, atmospheric data, and forest inventories indicate a historical carbon sink, and these apparent iCO2 responses are high in comparison to experiments and predictions from theory. Plant mortality and soil carbon iCO2 responses are highly uncertain. In conclusion, a range of evidence supports a positive terrestrial carbon sink in response to iCO2 , albeit with uncertain magnitude and strong suggestion of a role for additional agents of global change.

Towards a unified study of multiple stressors: divisions and common goals across research disciplines.

Anthropogenic environmental changes, or 'stressors', increasingly threaten biodiversity and ecosystem functioning worldwide. Multiple-stressor research is a rapidly expanding field of science that seeks to understand and ultimately predict the interactions between stressors. Reviews and meta-analyses of the primary scientific literature have largely been specific to either freshwater, marine or terrestrial ecology, or ecotoxicology. In this cross-disciplinary study, we review the state of knowledge within and among these disciplines to highlight commonality and division in multiple-stressor research. Our review goes beyond a description of previous research by using quantitative bibliometric analysis to identify the division between disciplines and link previously disconnected research communities. Towards a unified research framework, we discuss the shared goal of increased realism through both ecological and temporal complexity, with the overarching aim of improving predictive power. In a rapidly changing world, advancing our understanding of the cumulative ecological impacts of multiple stressors is critical for biodiversity conservation and ecosystem management. Identifying and overcoming the barriers to interdisciplinary knowledge exchange is necessary in rising to this challenge. Division between ecosystem types and disciplines is largely a human creation. Species and stressors cross these borders and so should the scientists who study them.

No carbon limitation after lower crown loss in Pinus radiata.

BACKGROUND AND AIMS: Biotic and abiotic stressors can cause different defoliation patterns within trees. Foliar pathogens of conifers commonly prefer older needles and infection with defoliation that progresses from the bottom crown to the top. The functional role of the lower crown of trees is a key question to address the impact of defoliation caused by foliar pathogens. METHODS: A 2 year artificial defoliation experiment was performed using two genotypes of grafted Pinus radiata to investigate the effects of lower-crown defoliation on carbon (C) assimilation and allocation. Grafts received one of the following treatments in consecutive years: control-control, control-defoliated, defoliated-control and defoliated-defoliated. RESULTS: No upregulation of photosynthesis either biochemically or through stomatal control was observed in response to defoliation. The root:shoot ratio and leaf mass were not affected by any treatment, suggesting prioritization of crown regrowth following defoliation. In genotype B, defoliation appeared to impose C shortage and caused reduced above-ground growth and sugar storage in roots, while in genotype A, neither growth nor storage was altered. Root C storage in genotype B decreased only transiently and recovered over the second growing season. CONCLUSIONS: In genotype A, the contribution of the lower crown to the whole-tree C uptake appears to be negligible, presumably conferring resilience to foliar pathogens affecting the lower crown. Our results suggest that there is no C limitation after lower-crown defoliation in P. radiata grafts. Further, our findings imply genotype-specific defoliation tolerance in P. radiata.

Modelling carbon sources and sinks in terrestrial vegetation.

Contents Summary 652 I. Introduction 652 II. Discrepancy in predicting the effects of rising [CO2 ] on the terrestrial C sink 655 III. Carbon and nutrient storage in plants and its modelling 656 IV. Modelling the source and the sink: a plant perspective 657 V. Plant-scale water and Carbon flux models 660 VI. Challenges for the future 662 Acknowledgements 663 Authors contributions 663 References 663 SUMMARY: The increase in atmospheric CO2 in the future is one of the most certain projections in environmental sciences. Understanding whether vegetation carbon assimilation, growth, and changes in vegetation carbon stocks are affected by higher atmospheric CO2 and translating this understanding in mechanistic vegetation models is of utmost importance. This is highlighted by inconsistencies between global-scale studies that attribute terrestrial carbon sinks to CO2 stimulation of gross and net primary production on the one hand, and forest inventories, tree-scale studies, and plant physiological evidence showing a much less pronounced CO2 fertilization effect on the other hand. Here, we review how plant carbon sources and sinks are currently described in terrestrial biosphere models. We highlight an uneven representation of complexity between the modelling of photosynthesis and other processes, such as plant respiration, direct carbon sinks, and carbon allocation, largely driven by available observations. Despite a general lack of data on carbon sink dynamics to drive model improvements, ways forward toward a mechanistic representation of plant carbon sinks are discussed, leveraging on results obtained from plant-scale models and on observations geared toward model developments.

Water relations determine short time leaf growth patterns in the mangrove Avicennia marina (Forssk.) Vierh.

High-resolution leaf growth is rarely studied despite its importance as a metric for plant performance and resource use efficiency. This is in part due to methodological challenges. Here, we present a method for in situ leaf growth measurements in a natural environment. We measured instantaneous leaf growth on a mature Avicennia marina subsp. australasica tree over several weeks. We measured leaf expansion by taking time-lapse images and analysing them using marker tracking software. A custom-made instrument was designed to enable long-term field studies. We detected a distinct diel growth pattern with leaf area shrinkage in the morning and leaf expansion in the afternoon and at night. On average, the observed daily shrinkage was 37% of the net growth. Most of the net growth occurred at night. Diel leaf area shrinkage and recovery continued after growth cessation. The amount of daily growth was negatively correlated with shrinkage, and instantaneous leaf growth and shrinkage were correlated with changes in leaf turgor. We conclude that, at least in this tree species, instantaneous leaf growth patterns are very strongly linked to, and most likely driven by, leaf water relations, suggesting decoupling of short-term growth patterns from carbon assimilation.

Partitioning direct and indirect effects reveals the response of water-limited ecosystems to elevated CO2.

Increasing concentrations of atmospheric carbon dioxide are expected to affect carbon assimilation and evapotranspiration (ET), ultimately driving changes in plant growth, hydrology, and the global carbon balance. Direct leaf biochemical effects have been widely investigated, whereas indirect effects, although documented, elude explicit quantification in experiments. Here, we used a mechanistic model to investigate the relative contributions of direct (through carbon assimilation) and indirect (via soil moisture savings due to stomatal closure, and changes in leaf area index) effects of elevated CO2 across a variety of ecosystems. We specifically determined which ecosystems and climatic conditions maximize the indirect effects of elevated CO2 The simulations suggest that the indirect effects of elevated CO2 on net primary productivity are large and variable, ranging from less than 10% to more than 100% of the size of direct effects. For ET, indirect effects were, on average, 65% of the size of direct effects. Indirect effects tended to be considerably larger in water-limited ecosystems. As a consequence, the total CO2 effect had a significant, inverse relationship with the wetness index and was directly related to vapor pressure deficit. These results have major implications for our understanding of the CO2 response of ecosystems and for global projections of CO2 fertilization, because, although direct effects are typically understood and easily reproducible in models, simulations of indirect effects are far more challenging and difficult to constrain. Our findings also provide an explanation for the discrepancies between experiments in the total CO2 effect on net primary productivity.

Invasive rodents have multiple indirect effects on seabird island invertebrate food web structure.

Burrowing seabirds that nest on islands transfer nutrients from the sea, disturb the soil through burrowing, damage tree foliage when landing, and thereby modify the surface litter. However, seabirds are in decline worldwide, as are their community- and ecosystem-level impacts, primarily due to invasive predatory mammals. The direct and indirect effects of seabird decline on communities and ecosystems are inherently complex. Here we employed network analysis, as a means of simplifying ecological complexity, to better understand the effects seabird loss may have on island invertebrate communities. Using data on leaf litter communities, we constructed invertebrate food webs for each of 18 offshore oceanic islands in northeastern New Zealand, nine of which have high seabird densities and nine of were invaded by rats. Ten network topological metrics (including entropy, generality, and vulnerability) were compared between rat-invaded and uninvaded (seabird-dominant) islands. We found that, on rat-invaded islands, the invertebrate food webs were smaller and less complex than on their seabird-dominated counterparts, which may be due to the suppression of seabird-derived nutrients and consequent effects on trophic cascades. This decreased complexity of food webs due to the presence of rats is indicative of lower ecosystem resistance via lower trophic redundancy. Our results show that rat effects on island ecosystems are manifested throughout entire food webs, and demonstrate how network analysis may be useful to assess ecosystem recovery status as these invaded islands are restored.

Phytophthora pluvialis Studies on Douglas-fir Require Swiss Needle Cast Suppression.

Phytophthora pluvialis is associated with early defoliation and shoot dieback in Douglas-fir in Oregon and New Zealand. In 2013, P. pluvialis was described from mixed tanoak-Douglas-fir forests in the Pacific Northwest and concurrently recognized as the main causal agent of red needle cast (RNC) in New Zealand radiata pine plantations. Little is known about its infection cycle and impact on host physiology. P. pluvialis studies in Douglas-fir are challenging due to the ubiquitous presence of the endophyte Phaeocryptopus gaeumannii, which produces similar symptoms and premature defoliation with persistent needle wetness, known as Swiss needle cast (SNC). Nonetheless, our study showed P. pluvialis infection in the presence of SNC. Exclusive expression of P. pluvialis is difficult to achieve as both diseases are promoted by high humidity. Here we established a 'dry leaf' strategy to suppress SNC when inoculating Douglas-fir needles for RNC studies. Sheltering plants along with drip irrigation to avoid needle wetness during the P. gaeumannii sporulation period suppressed its development in the new season flush. The diminished endophyte inoculum enabled bias-reduced studies of P. pluvialis impacts on Douglas-fir without the confounding effects of stomatal blockage and premature defoliation caused by P. gaeumannii.

Long-term ¹³C labeling provides evidence for temporal and spatial carbon allocation patterns in mature Picea abies.

There is evidence of continued stimulation of foliage photosynthesis in trees exposed to elevated atmospheric CO2 concentrations; however, this is mostly without a proportional growth response. Consequently, we lack information on the fate of this extra carbon (C) acquired. By a steady application of a (13)CO2 label in a free air CO2 enrichment (FACE) experiment, we traced the fate of C in 37-m-tall, ca. 110-year-old Picea abies trees in a natural forest in Switzerland. Hence, we are not reporting tree responses to elevated CO2 (which would require equally (13)C labeled controls), but are providing insights into assimilate processing in such trees. Sunlit needles and branchlets grow almost exclusively from current assimilates, whereas shaded parts of the crowns also rely on stored C. Only 2.5 years after FACE initiation, tree rings contained 100% new C. Stem-respiratory CO2 averaged 50% of new C over the entire FACE period. Fine roots and mycorrhizal fungi contained 49-56 and 26-43% new C, respectively, after 2.5 years. The isotopic signals in soil CO2 arrived 12 days after the onset of FACE, yet it contained only ca. 15% new C thereafter. We conclude that new C first feeds into fast turnover C pools in the canopy and becomes increasingly mixed with older C sources as one moves away (downward) from the crown. We speculate that enhanced C turnover (its metabolic cost) along the phloem path, as evidenced by basipetal isotope signal depletion, explains part of the 'missing carbon' in trees that assimilated more C under elevated CO2.

Beyond global change: lessons from 25 years of CO2 research.

Over the past 25 years, countless experiments have been conducted on the impact of increased atmospheric CO2 concentration on various plants and ecosystems. While this research was motivated to better understand and predict how rising CO2 will affect the structure and function of ecosystems in the future, it also shed light on some general, CO2-research independent, aspects in ecological research. Interestingly, it is these general aspects that continue to create confusion and lead to misinterpretation. Here, we focus on seven interrelated key issues including (1) the confusion between fluxes and pools, (2) the stoichiometric aspects of growth and biomass production, (3) resource allocation within organisms, (4) data scaling and the choice of a reference metric, (5) the consideration of time and timing (experimental duration, ontogenetic shifts), (6) confounding and second-order (indirect or feedback) effects, and (7) the key role of biodiversity. The principles deriving from addressing these issues relate strongly to each other. Their concurrent consideration requires experimenters and modellers to likewise maintain a broad, holistic perspective. In this synthesis, we attempt to show how appropriate consideration of these principles can greatly enhance the assessment of the validity, plausibility and generality of experimental and modelling results. We conclude that neglecting to adequately address these key issues in ecological research may lead to overestimations of measured responses and/or simplistic interpretations. Our examples mostly originate from research on plant responses to elevated atmospheric CO2, but are also applicable to other areas of ecological research. We provide a checklist for the planning of ecological field experiments and the interpretation of their results that may help in avoiding common pitfalls.

Precipitation manipulation experiments--challenges and recommendations for the future.

Climatic changes, including altered precipitation regimes, will affect key ecosystem processes, such as plant productivity and biodiversity for many terrestrial ecosystems. Past and ongoing precipitation experiments have been conducted to quantify these potential changes. An analysis of these experiments indicates that they have provided important information on how water regulates ecosystem processes. However, they do not adequately represent global biomes nor forecasted precipitation scenarios and their potential contribution to advance our understanding of ecosystem responses to precipitation changes is therefore limited, as is their potential value for the development and testing of ecosystem models. This highlights the need for new precipitation experiments in biomes and ambient climatic conditions hitherto poorly studied applying relevant complex scenarios including changes in precipitation frequency and amplitude, seasonality, extremity and interactions with other global change drivers. A systematic and holistic approach to investigate how soil and plant community characteristics change with altered precipitation regimes and the consequent effects on ecosystem processes and functioning within these experiments will greatly increase their value to the climate change and ecosystem research communities. Experiments should specifically test how changes in precipitation leading to exceedance of biological thresholds affect ecosystem resilience and acclimation.

Simple additive effects are rare: a quantitative review of plant biomass and soil process responses to combined manipulations of CO2 and temperature.

In recent years, increased awareness of the potential interactions between rising atmospheric CO2 concentrations ([ CO2 ]) and temperature has illustrated the importance of multifactorial ecosystem manipulation experiments for validating Earth System models. To address the urgent need for increased understanding of responses in multifactorial experiments, this article synthesizes how ecosystem productivity and soil processes respond to combined warming and [ CO2 ] manipulation, and compares it with those obtained in single factor [ CO2 ] and temperature manipulation experiments. Across all combined elevated [ CO2 ] and warming experiments, biomass production and soil respiration were typically enhanced. Responses to the combined treatment were more similar to those in the [ CO2 ]-only treatment than to those in the warming-only treatment. In contrast to warming-only experiments, both the combined and the [ CO2 ]-only treatments elicited larger stimulation of fine root biomass than of aboveground biomass, consistently stimulated soil respiration, and decreased foliar nitrogen (N) concentration. Nonetheless, mineral N availability declined less in the combined treatment than in the [ CO2 ]-only treatment, possibly due to the warming-induced acceleration of decomposition, implying that progressive nitrogen limitation (PNL) may not occur as commonly as anticipated from single factor [ CO2 ] treatment studies. Responses of total plant biomass, especially of aboveground biomass, revealed antagonistic interactions between elevated [ CO2 ] and warming, i.e. the response to the combined treatment was usually less-than-additive. This implies that productivity projections might be overestimated when models are parameterized based on single factor responses. Our results highlight the need for more (and especially more long-term) multifactor manipulation experiments. Because single factor CO2 responses often dominated over warming responses in the combined treatments, our results also suggest that projected responses to future global warming in Earth System models should not be parameterized using single factor warming experiments.

The Who or the How? Species vs. Ecosystem Function Priorities in Conservation Ecology.

Current conservation strategies are targeted at preserving species, without explicitly aiming at the maintenance of ecosystem functions. In a physically highly connected world, the unintentional relocation of terrestrial, marine, and microbial life is therefore unavoidable and has been an integral part of human evolution for thousands of years. Here, we challenge the default perception often shared among conservation ecologists that preserving native species at all costs and reducing the number of exotic species and their abundance is the only way to conservation and restoration success. While this strategy is valuable in cases where exotic species disrupt ecological function, there are examples where exotic species have similar functional traits to the threatened or extinct native species and can in fact help maintain the overall or target function of an ecosystem. In the race to cope with global environmental change, we argue that ecosystem function and ecosystem services need to be viewed not only through a taxonomic lens, but increasingly also through a functional, trait-based one.

Disentangling the net: concomitant xylem and over-bark size measurements reveal the phloem-generated turgor signal behind daytime stem swelling in the mangrove Avicennia marina.

Daytime stem shrinking is a well recorded phenomenon: trees dip into their internal water stores to meet imbalances between water supply and demand. Uncertainty surrounds the mechanisms behind the unusual pattern of daytime stem swelling, presented by species like the mangrove Avicennia marina (Forssk.) Vierh., and which is thought to originate in the osmotic adjustment of storage tissues. We performed on-xylem radius change (XRC) and whole-stem radius change (SRC) measurements with point dendrometers to ascertain if the swelling of the stem is due to an increase in the thickness of the phloem and inner-bark (BRC). We measured leaf water potential (ψleaf), sap flow, leaf turgor and microclimate to understand the coupling between BRC and transpiration-driven changes in XRC. Our results present direct evidence of the type of mechanism responsible for daytime stem swelling. Inner-bark thickness increase concurrent with XRC decrease, sap-flow increase and leaf turgor loss, reveals a phloem-generated turgor signal behind daytime stem swelling of tree stems. On-xylem measurements were highly heterogeneous due to the variability in the three dimensional fish-net wood structure of the stem of A. marina. As daytime decreases in XRC were compensated by BRC and correlated with conditions of high water demand, we suggest a potential role of daytime stem swelling in the hydraulic safety of A. marina.

Globally consistent influences of seasonal precipitation limit grassland biomass response to elevated CO2.

Rising atmospheric carbon dioxide concentration should stimulate biomass production directly via biochemical stimulation of carbon assimilation, and indirectly via water savings caused by increased plant water-use efficiency. Because of these water savings, the CO2 fertilization effect (CFE) should be stronger at drier sites, yet large differences among experiments in grassland biomass response to elevated CO2 appear to be unrelated to annual precipitation, preventing useful generalizations. Here, we show that, as predicted, the impact of elevated CO2 on biomass production in 19 globally distributed temperate grassland experiments reduces as mean precipitation in seasons other than spring increases, but that it rises unexpectedly as mean spring precipitation increases. Moreover, because sites with high spring precipitation also tend to have high precipitation at other times, these effects of spring and non-spring precipitation on the CO2 response offset each other, constraining the response of ecosystem productivity to rising CO2. This explains why previous analyses were unable to discern a reliable trend between site dryness and the CFE. Thus, the CFE in temperate grasslands worldwide will be constrained by their natural rainfall seasonality such that the stimulation of biomass by rising CO2 could be substantially less than anticipated.

A meta-analysis of 1,119 manipulative experiments on terrestrial carbon-cycling responses to global change.

Direct quantification of terrestrial biosphere responses to global change is crucial for projections of future climate change in Earth system models. Here, we synthesized ecosystem carbon-cycling data from 1,119 experiments performed over the past four decades concerning changes in temperature, precipitation, CO2 and nitrogen across major terrestrial vegetation types of the world. Most experiments manipulated single rather than multiple global change drivers in temperate ecosystems of the USA, Europe and China. The magnitudes of warming and elevated CO2 treatments were consistent with the ranges of future projections, whereas those of precipitation changes and nitrogen inputs often exceeded the projected ranges. Increases in global change drivers consistently accelerated, but decreased precipitation slowed down carbon-cycle processes. Nonlinear (including synergistic and antagonistic) effects among global change drivers were rare. Belowground carbon allocation responded negatively to increased precipitation and nitrogen addition and positively to decreased precipitation and elevated CO2. The sensitivities of carbon variables to multiple global change drivers depended on the background climate and ecosystem condition, suggesting that Earth system models should be evaluated using site-specific conditions for best uses of this large dataset. Together, this synthesis underscores an urgent need to explore the interactions among multiple global change drivers in underrepresented regions such as semi-arid ecosystems, forests in the tropics and subtropics, and Arctic tundra when forecasting future terrestrial carbon-climate feedback.