Stable isotope analysis is a powerful tool for assessing plant carbon and water relations and their impact on biogeochemical processes at different scales. Our process-based understanding of stable ...isotope signals, as well as technological developments, has progressed significantly, opening new frontiers in ecological and interdisciplinary research. This has promoted the broad utilisation of carbon, oxygen and hydrogen isotope applications to gain insight into plant carbon and water cycling and their interaction with the atmosphere and pedosphere. Here, we highlight specific areas of recent progress and new research challenges in plant carbon and water relations, using selected examples covering scales from the leaf to the regional scale. Further, we discuss strengths and limitations of recent technological developments and approaches and highlight new opportunities arising from unprecedented temporal and spatial resolution of stable isotope measurements.
• Mediterranean‐type ecosystems contain 20% of all vascular plant diversity on Earth and have been identified as being particularly threatened by future increases in drought. Of particular concern is ...the Cape Floral Region of South Africa, a global biodiversity hotspot, yet there are limited experimental data to validate predicted impacts on the flora. In a field rainout experiment, we tested whether rooting depth and degree of isohydry or anisohydry could aid in the functional classification of drought responses across diverse growth forms. • We imposed a 6‐month summer drought, for 2 yr, in a mountain fynbos shrubland. We monitored a suite of parameters, from physiological traits to morphological outcomes, in seven species comprising the three dominant growth forms (deep‐rooted proteoid shrubs, shallow‐rooted ericoid shrubs and graminoid restioids). • There was considerable variation in drought response both between and within the growth forms. The shallow‐rooted, anisohydric ericoid shrubs all suffered considerable reductions in growth and flowering and increased mortality. By contrast, the shallow‐rooted, isohydric restioids and deep‐rooted, isohydric proteoid shrubs were largely unaffected by the drought. • Rooting depth and degree of iso/anisohydry allow a first‐order functional classification of drought response pathways in this flora. Consideration of additional traits would further refine this approach.
ABSTRACT
Fog is a defining feature of the coastal California redwood forest and fog inputs via canopy drip in summer can constitute 30% or more of the total water input each year. A great deal of ...occult precipitation (fog and light rain) is retained in redwood canopies, which have some of the largest leaf area indices known (Westman & Whittaker, Journal of Ecology 63, 493–520, 1975). An investigation was carried out to determine whether some fraction of intercepted fog water might be directly absorbed through leaf surfaces and if so, the importance of this to the water relations physiology of coast redwood, Sequoia sempervirens. An array of complimentary techniques were adopted to demonstrate that fog is absorbed directly by S. sempervirens foliage. Xylem sap transport reversed direction during heavy fog, with instantaneous flow rates in the direction of the soil peaking at approximately 5–7% of maximum transpiration rate. Isotopic analyses showed that up to 6% of a leaf's water content could be traced to a previous night's fog deposition, but this amount varied considerably depending on the age and water status of the leaves. Old leaves, which appear most able to absorb fog water were able to absorb distilled water when fully submersed at an average rate of 0.90 mmol m2 s−1, or about 80% of transpiration rates measured at the leaf level in the field. Sequoia sempervirens has poor stomatal control in response to a drying atmosphere, with rates of water loss on very dry nights up to 40% of midday summer values and rates above 10% being extremely common. Owing to this profligate water use behaviour of S. sempervirens, it appears that fog has a greater role in suppressing water loss from leaves, and thereby ameliorating daily water stress, than in providing supplemental water to foliar tissues per se. Although direct foliar absorption from fog inputs represents only a small fraction of the water used each day, fog's in reducing transpiration and rehydrating leaf tissues during the most active growth periods in summer may allow for greater seasonal carbon fixation and thus contribute to the very fast growth rates and great size of this species.
Fine root (<2 mm) cycling rates are important for understanding plant ecology and carbon fluxes in forests, but they are difficult to determine and remain uncertain. This paper synthesizes ...minirhizotron and isotopic data and a root model and concludes that (1) fine roots have a spectrum of turnover times ranging from months to many years and (2) the mean age of live root biomass (A) and the mean age of roots when they die (i.e., their turnover time (τ)) are not equal. We estimated A and τ of fine roots in three forests using the root model Radix. For short‐lived roots, we constrained τ with existing minirhizotron data; for long‐lived roots, we used new radiocarbon measurements of roots sampled by diameter size class and root branch order. Long‐lived root pools had site mean τ of 8–13 y and 5–9 y when sampled by diameter and branch order, respectively. Mean turnover times across sites were in general not significantly different as a function of branch‐order, size class, or depth. Our modeling results indicate that ∼20% of fine root biomass has turnover times of about a year, and ∼80% has decadal turnover times. This partitioning is reflected in our predicted mean ages of ∼9 y and turnover times of ∼3 y. We estimate that fine root mortality contributes between 38 and 104 g C m−2 y−1 to soil in these forests. These estimates are 20 to 80% of previous estimates in these and similar forests, in part because we explicitly account for the large portion of fine‐root biomass with decadal cycling rates. Our work shows that both fast and slow cycling roots must be modeled jointly to account for the heterogeneous nature of fine‐root dynamics.
The spatiotemporal dynamics of plant water sources are hidden and poorly understood. We document water source use of Quercus garryana growing in Northern California on a profile of approximately 50 ...cm of soil underlain by 2–4 m of weathered bedrock (sheared shale mélange) that completely saturates in winter, when the oaks lack leaves, and progressively dries over the summer. We determined oak water sources by combining observations of water stable isotope composition, vadose zone moisture and groundwater dynamics, and metrics of tree water status (potential) and use (sapflow). During the spring, oak xylem water is isotopically similar to the seasonal groundwater and shallow, evaporatively enriched soil moisture pools. However, as soils dry and the water table recedes to the permanently saturated, anoxic, low‐conductivity fresh bedrock boundary, Q. garryana shifts to using a water source with a depleted isotopic composition that matches residual moisture in the deep soil and underlying weathered bedrock vadose zone. Sapflow rates remain high as late‐summer predawn water potentials drop below −2.5 MPa. Neutron probe surveys reveal late‐summer rock moisture declines under the oaks in contrast to constant rock moisture levels under grass‐dominated areas. We therefore conclude that the oaks temporarily use seasonal groundwater when it occupies the weathered profile but otherwise use deep unsaturated zone moisture after seasonal groundwater recedes. The ample moisture, connected porosity, and oxygenated conditions of the weathered bedrock vadose zone make it a key tree water resource during the long summer dry season of the local Mediterranean climate.
Plain Language Summary
What are the water sources that allow oaks to transpire through extended dry periods? Oaks in California are thought to tap into groundwater to meet dry season water demand. Here, we show that oaks growing in a savanna woodland instead use tightly held moisture within deep soil and weathered bedrock above the saturated zone. We determined this by matching stable isotopes in the trees' water to these moisture pools. Deep soil and rock moisture were isotopically lighter than shallow soil moisture, which was affected by evaporative enrichment, and the groundwater, which looked more like average wet season rainfall. Monitored moisture declines within the weathered bedrock corroborate the isotopic interpretation that rock moisture sustained oak transpiration. Although the saturated zone was only a few meters below the ground surface in late summer, the trees did not use it due to its low oxygen content and residence in low permeability fresh bedrock. Our findings matter to forest management because of the need to determine when and where trees use groundwater, which regulates ecologically critical baseflow. Moisture extraction from the weathered bedrock unsaturated zone is likely important globally, as forests are widespread on hillslopes with thin soils overlying weathered bedrock.
Key Points
Isotopic, physiologic, and hydrologic observations were combined to identify oak water sources
Rock and deep soil moisture rather than groundwater sustain transpiration in summer dry season
Deep unsaturated zone moisture sources and oak water were isotopically depleted
Fog has been viewed as an important source of moisture in many coastal ecosystems, yet its importance for the plants which inhabit these ecosystems is virtually unknown. Here, I report the results of ...a 3-year investigation of fog inputs and the use of fog water by plants inhabiting the heavily fog inundated coastal redwood (Sequoia sempervirens) forests of northern California. During the study period, 34%, on average, of the annual hydrologic input was from fog drip off the redwood trees themselves (interception input). When trees were absent, the average annual input from fog was only 17%, demonstrating that the trees significantly influence the magnitude of fog water input to the ecosystem. Stable hydrogen and oxygen isotope analyses of water from fog, rain, soil water, and xylem water extracted from the dominant plant species were used to characterize the water sources used by the plants. An isotopic mixing model was employed to then quantify how much fog water each plant used each month during the 3-year study. In summer, when fog was most frequent, ∼19% of the water within S. sempervirens, and ∼66% of the water within the understory plants came from fog after it had dripped from tree foliage into the soil; for S. sempervirens, this fog water input comprised 13-45% of its annual transpiration. For all plants, there was a significant reliance on fog as a water source, especially in summer when rainfall was absent. Dependence on fog as a moisture source was highest in the year when rainfall was lowest but fog inputs normal. Interestingly, during the mild El Niño year of 1993, when the ratio of rainfall to fog water input was significantly higher and fog inputs were lower, both the proportion and coefficient of variation in how much fog water was used by plants increased. An explanation for this is that while fog inputs were lower than normal in this El Niño year, they came at a time when plant demand for water was highest (summer). Therefore, proportional use of fog water by plants increased. The results presented suggest that fog, as a meteorological factor, plays an important role in the water relations of the plants and in the hydrology of the forest. These results demonstrate the importance of understanding the impacts of climatic factors and their oscillations on the biota. The results have important implications for ecologists, hydrologists, and forest managers interested in fog-inundated ecosystems and the plants which inhabit them.
It is commonly assumed that transpiration does not occur at night because leaf stomata are closed in the dark. We tested this assumption across a diversity of ecosystems and woody plant species by ...various methods to explore the circumstances when this assumption is false. Our primary goals were: (1) to evaluate the nature and magnitude of nighttime transpiration, En, or stomatal conductance, gn; and (2) to seek potential generalizations about where and when it occurs. Sap-flow, porometry and stable isotope tracer measurements were made on 18 tree and eight shrub species from seven ecosystem types. Coupled with environmental data, our findings revealed that most of these species transpired at night. For some species and circumstances, nighttime leaf water loss constituted a significant fraction of total daily water use. Our evidence shows that En or gn can occur in all but one shrub species across the systems we investigated. However, under conditions of high nighttime evaporative demand or low soil water availability, stomata were closed and En or gn approached zero in eleven tree and seven shrub species. When soil water was available, En or gn was measurable in these same species demonstrating plasticity for En or gn. We detected En or gn in both trees and shrubs, and values were highest in plants from sites with higher soil water contents and in plants from ecosystems that were less prone to atmospheric or soil water deficits. Irrespective of plant or ecosystem type, many species showed En or gn when soil water deficits were slight or non-existent, or immediately after rainfall events that followed a period of soil water deficit. The strongest relationship was between En or gn and warm, low humidity and (or) windy (> 0.8 m s(-1)) nights when the vapor pressure deficit remained high (> 0.2 kPa in wet sites, > 0.7 kPa in dry sites). Why En or gn occurs likely varies with species and ecosystem type; however, our data support four plausible explanations: (1) it may facilitate carbon fixation earlier in the day because stomata are already open; (2) it may enhance nutrient supply to distal parts of the crown when these nutrients are most available (in wet soils) and transport is rapid; (3) it may allow for the delivery of dissolved O2 via the parenchyma to woody tissue sinks; or (4) it may occur simply because of leaky cuticles in older leaves or when stomata cannot close fully because of obstructions from stomatal (waxy) plugs, leaf endophytes or asymmetrical guard cells (all non-adaptive reasons). We discuss the methodological, ecophysiological, and theoretical implications of the occurrence of En or gn for investigations at a variety of scales.
Plant water stress in response to rainfall variability is mediated by subsurface water storage, yet the controls on stored plant‐available water remain poorly understood. Here we develop a ...probabilistic water balance model for Mediterranean climates that relates the amount of water stored over the wet season to annual rainfall statistics and subsurface storage capacity in soil and weathered bedrock. This model predicts that low storage capacity—relative to winter rainfall—results in similar year‐to‐year summer water availability, as both relatively wet and dry winters replenish storage. Observed water balances in seven catchments in the Northern California Coast Ranges exhibited this dynamic. We hypothesized that plants would be decoupled from precipitation variability at these storage‐capacity‐limited sites and observed that summer productivity and water use (inferred from the enhanced vegetation index) were independent of winter rainfall totals. These areas emerged largely unscathed from recent extreme drought, despite widespread plant mortality elsewhere.
Plain Language Summary
When does a shortage of precipitation become a shortage of water supply to plants? In rain‐dominated seasonally dry climates, the answer depends on how water is stored belowground. Here we propose—perhaps counterintuitively—that low water storage capacity in Earth's critical zone (which includes soil and weathered bedrock) relative to average rainfall can decouple plant community productivity and water use from rainfall variability, and conversely that relatively large storage capacity increases plant sensitivity to annual swings in rainfall totals. A simple model and analysis of watersheds in winter wet, summer dry climates in California reveal that where it consistently rains much more than the subsurface can store, a similar amount of water is stored belowground in both relatively wet and dry years, with excess rainfall leaving as runoff. We hypothesized that this would result in similar year‐to‐year summer plant water availability, in spite of highly variable winter rainfall. We found, via satellite observations, that summer plant greenness was insensitive to swings in precipitation at these “storage‐capacity‐limited” sites. Contrary to predictions based primarily on tree density and rainfall deficits, these sites did not experience widespread mortality in the 2011‐2016 extreme drought.
Key Points
Where annual rainfall reliably exceeds subsurface storage capacity, plant productivity should be insensitive to rainfall variability
Water balances reveal sites where storage is replenished in both wet and dry winters, resulting in consistent summer plant water supply
Such storage‐capacity limited sites are inherently resilient to meteorological drought
At the leaf scale, it is a long-held assumption that stomata close at night in the absence of light, causing transpiration to decrease to zero. Energy balance models and evapotranspiration equations ...often rely on net radiation as an upper bound, and some models reduce evapotranspiration to zero at night when there is no solar radiation. Emerging research is showing, however, that transpiration can occur throughout the night in a variety of vegetation types and biomes. At the ecosystem scale, eddy covariance measurements have provided extensive data on latent heat flux for a multitude of ecosystem types globally. Nighttime eddy covariance measurements, however, are generally unreliable because of low turbulence. If significant nighttime water loss occurs, eddy flux towers may be missing key information on latent heat flux. We installed and measured rates of sap flow by the heat ratio method (Burgess et al. 2001) at two AmeriFlux (part of FLUXNET) sites in California. The heat ratio method allows measurement and quantification of low rates of sap flow, including negative rates (i.e., hydraulic lift). We measured sap flow in five Pinus ponderosa Dougl. ex Laws. trees and three Arctostaphylos manzanita Parry and two Ceanothus cordulatus A. Kellog shrubs in the Sierra Nevada Mountains, and in five Quercus douglasii Hook and Arn. trees at an oak savanna in the Central Valley of California. Nocturnal sap flow was observed in all species, and significant nighttime water loss was observed in both species of trees. Vapor pressure deficit and air temperature were both well correlated with nighttime transpiration; the influence of wind speed on nighttime transpiration was insignificant at both sites. We distinguished between storage-tissue refilling and water loss based on data from Year 2005, and calculated the percentage by which nighttime transpiration was underestimated by eddy covariance measurements at both sites.
Tropical dry forests (TDFs) undergo a substantial dry season in which plant species must endure several months of drought. Although TDFs support a diverse array of plant growth forms, it is not clear ...how they vary in mechanisms for coping with seasonal drought. We measured organic tissue stable isotopic composition of carbon (δ13C) and nitrogen (δ15N) across six plant growth forms including epiphytes, terrestrial succulents, trees, shrubs, herbs, and vines, and oxygen (δ18O) of four growth forms, to distinguish among patterns of resource acquisition and evaluate mechanisms for surviving annual drought in a lowland tropical dry forest in Yucatan, Mexico. Terrestrial succulent and epiphyte δ13C was around -14‰, indicating photosynthesis through the Crassulacean acid metabolism pathway, and along with one C4 herb were distinct from mean values of all other growth forms, which were between -26 and -29‰ indicating C3 photosynthesis. Mean tissue δ15N across epiphytes was -4.95‰ and was significantly lower than all other growth forms, which had values around +3‰. Tissue N concentration varied significantly among growth forms with epiphytes and terrestrial succulents having significantly lower values of about 1% compared to trees, shrubs, herbs and vines, which were around 3%. Tissue C concentration was highest in trees, shrubs and vines, intermediate in herbs and epiphytes and lowest in terrestrial succulents. δ18O did not vary among growth forms. Overall, our results suggest several water-saving aspects of resource acquisition, including the absolute occurrence of CAM photosynthesis in terrestrial succulents and epiphytes, high concentrations of leaf N in some species, which may facilitate CO2 drawdown by photosynthetic enzymes for a given stomatal conductance, and potentially diverse N sources ranging from atmospheric N in epiphytes with extremely depleted δ15N values, and a large range of δ15N values among trees, many of which are legumes and dry season deciduous.
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