Barbara J. Bond

Age-related changes in photosynthesis of woody plants

Woody peoffnials do not appear to go through a defined senescence phase but do have predictable developmental stages. Reduced photosynthesis and stomatal conductance have been reported at all developmental transitions, although some studies have shown the opposite. What causes these changes and why do results differ among studies? Do these changes result from or cause changes in growth? What are the roles of genetics, size, changing conditions and cumulative environmental stress in aging trees? Definitive answers remain elusive but recent research is helping to clarify some of the processes associated with aging and to point the way for further study.

Foliage physiology and biochemistry in response to light gradients in conifers with varying shade tolerance

Abstract To examine the predictability of leaf physiology and biochemistry from light gradients within canopies, we measured photosynthetic light-response curves, leaf mass per area (LMA) and concentrations of nitrogen, phosphorus and chlorophyll at 15–20 positions within canopies of three conifer species with increasing shade tolerance, ponderosa pine [Pinus ponderosa (Laws.)], Douglas fir [Pseudotsuga menziesii (Mirb.) Franco], and western hemlock [Tsuga heterophylla (Raf.) Sarg.]. Adjacent to each sampling position, we continuously monitored photosynthetically active photon flux density (PPFD) over a 5-week period using quantum sensors. From these measurements we calculated FPAR: integrated PPFD at each sampling point as a fraction of full sun. From the shadiest to the brightest canopy positions, LMA increased by about 50% in ponderosa pine and 100% in western hemlock; Douglas fir was intermediate. Canopy-average LMA increased with decreasing shade tolerance. Most foliage properties showed more variability within and between canopies when expressed on a leaf area basis than on a leaf mass basis, although the reverse was true for chlorophyll. Where foliage biochemistry or physiology was correlated with FPAR, the relationships were non-linear, tending to reach a plateau at about 50% of full sunlight. Slopes of response functions relating physiology and biochemistry to ln(FPAR) were not significantly different among species except for the light compensation point, which did not vary in response to light in ponderosa pine, but did in the other two species. We used the physiological measurements for Douglas fir in a model to simulate canopy photosynthetic potential (daily net carbon gain limited only by PPFD) and tested the hypothesis that allocation of carbon and nitrogen is optimized relative to PPFD gradients. Simulated photosynthetic potential for the whole canopy was slightly higher (<10%) using the measured allocation of C and N within the canopy compared with no stratification (i.e., all foliage identical). However, there was no evidence that the actual allocation pattern was optimized on the basis of PPFD gradients alone; simulated net carbon assimilation increased still further when even more N and C were allocated to high-light environments at the canopy top.

Net Ecosystem Exchanges of Carbon, Water, and Energy in Young and Old-growth Douglas-Fir Forests

To be able to estimate the cumulative carbon budget at broader scales, it is essential to understand net ecosystem exchanges (NEE) of carbon and water in various ages and types of ecosystems. Using eddy-covariance (EC) in Douglas-fir dominated forests in the Wind River Valley, Washington, USA, we measured NEE of carbon, water, and energy from July through September in a 40-year-old stand (40YR) in 1998, a 20-year-old stand (20YR) in 1999, and a 450-year-old stand (450YR) during both years. All three stands were net carbon sinks during the dry, warm summers, with mean net daily accumulation of –0.30 g C m−2 d−1, –2.76 g C m−2 d−1, and –0.38 g C m−2 d−1, respectively, in the 20YR, 40YR, and 450YR (average of 1998, 1999) stands; but for individual years, the 450YR stand was a carbon source in 1998 (0.51 g C m−2 d−1) and a sink in 1999 (–1.26 g C m−2 d−1). The interannual differences for the summer months were apparent for cumulative carbon exchange at the 450YR stand, which had 46.9 g C m−2 loss in 1998 and 115.9 g C m−2 gain in 1999. As predicted, the 40YR stand assimilated the most carbon and lost the least amount of water to the atmosphere through evapotranspiration.

Environmental sensitivity of gas exchange in different-sized trees.

The carbon isotope signature (δ13C) of foliar cellulose from sunlit tops of trees typically becomes enriched as trees of the same species in similar environments grow taller, indicative of size-related changes in leaf gas exchange. However, direct measurements of gas exchange in common environmental conditions do not always reveal size-related differences, even when there is a distinct size-related trend in δ13C of the very foliage used for the gas exchange measurements. Since δ13C of foliage predominately reflects gas exchange during spring when carbon is incorporated into leaf cellulose, this implies that gas exchange differences in different-sized trees are most likely to occur in favorable environmental conditions during spring. If gas exchange differs with tree size during wet but not dry conditions, then this further implies that environmental sensitivity of leaf gas exchange varies as a function of tree size. These implications are consistent with theoretical relationships among height, hydraulic conductance and gas exchange. We investigated the environmental sensitivity of gas exchange in different-sized Douglas-fir (Pseudotsuga menziesii) via a detailed process model that specifically incorporates size-related hydraulic conductance [soil–plant–atmosphere (SPA)], and empirical measurements from both wet and dry periods. SPA predicted, and the empirical measurements verified, that differences in gas exchange associated with tree size are greatest in wet and mild environmental conditions and minimal during drought. The results support the hypothesis that annual net carbon assimilation and transpiration of trees are limited by hydraulic capacity as tree size increases, even though at particular points in time there may be no difference in gas exchange between different-sized trees. Maximum net ecosystem exchange occurs in spring in Pacific Northwest forests; therefore, the presence of hydraulic limitations during this period may play a large role in carbon uptake differences with stand-age. The results also imply that the impacts of climate change on the growth and physiology of forest trees will vary depending on the age and size of the forest.

Applying the dual-isotope conceptual model to interpret physiological trends under uncontrolled conditions

The inter-relationships among δ(13)C and δ(18)O in tree ring cellulose and ring width have the potential to illuminate long-term physiological and environmental information in forest stands that have not been monitored. We examine how within-stand competition and environmental gradients affect ring widths and the stable isotopes of cellulose. We utilize a natural climate gradient across a catchment dominated by Douglas-fir and temporal changes in climate over an 8-year period. We apply a dual-isotope approach to infer physiological response of trees in differing crown dominance classes to temporal and spatial changes in environmental conditions using a qualitative conceptual model of the (13)C-(18)O relationship and by normalizing the data to minimize other variance. The δ(13)C and δ(18)O of cellulose were correlated with year-to-year variation in relative humidity and consistent with current isotope theory. Using a qualitative conceptual model of the (13)C-(18)O relationship and physiological knowledge about the species, we interpreted these changes as stomatal conductance responses to evaporative demand. Spatial variance between plots was not strong and seemed related to leaf nitrogen rather than any other environmental variable. Dominant trees responded to environmental gradients more consistently with current isotope theory as compared with other classes within the same stand. We found a correlation of stable isotopes with environmental variables is useful for assessing the impacts of environmental change over short time series and where growth varies only minimally with climate.

Relationships Between Tree Height and Carbon Isotope Discrimination

Understanding how tree size impacts leaf- and crown-level gas exchange is essential to predicting forest yields and carbon and water budgets. The stable carbon isotope ratio (δ13C) of organic matter has been used to examine the relationship of gas exchange to tree size for a host of species because it carries a temporally integrated signature of foliar photosynthesis and stomatal conductance. The carbon isotope composition of leaves reflects discrimination against 13C relative to 12C during photosynthesis and is the net result of the balance of change in CO2 supply and demand at the sites of photosynthesis within the leaf mesophyll. Interpreting the patterns of changes in δ13C with tree size are not always clear, however, because multiple factors that regulate gas exchange and carbon isotope discrimination (Δ) co-vary with height, such as solar irradiance and hydraulic conductance. Here we review 36 carbon isotope datasets from 38 tree species and conclude that there is a consistent, linear decline of Δ with height. The most parsimonious explanation of this result is that gravitational constraints on maximum leaf water potential set an ultimate boundary on the shape and sign of the relationship. These hydraulic constraints are manifest both over the long term through impacts on leaf structure, and over diel periods via impacts on stomatal conductance, photosynthesis and leaf hydraulic conductance. Shading induces a positive offset to the linear decline, consistent with light limitations reducing carbon fixation and increasing partial pressures of CO2 inside of the leaf, p c at a given height. Biome differences between tropical and temperate forests were more important in predicting Δ and its relationship to height than wood type associated with being an angiosperm or gymnosperm. It is not yet clear how leaf internal conductance varies with leaf mass area, but some data in particularly tall, temperate conifers suggest that photosynthetic capacity may not vary dramatically with height when compared between tree-tops, while stomatal and leaf internal conductances do decline in unison with height within canopy gradients. It is also clear that light is a critical variable low in the canopy, whereas hydrostatic constraints dominate the relationship between Δ and height in the upper canopy. The trend of increasing maximum height with decreasing minimum Δ suggests that trees that become particularly tall may be adapted to tolerate particularly low values of p c.

USING NOCTURNAL COLD AIR DRAINAGE FLOW TO MONITOR ECOSYSTEM PROCESSES IN COMPLEX TERRAIN

This paper presents initial investigations of a new approach to monitor ecosystem processes in complex terrain on large scales. Metabolic processes in mountainous ecosystems are poorly represented in current ecosystem monitoring campaigns because the methods used for monitoring metabolism at the ecosystem scale (e.g., eddy covariance) require flat study sites. Our goal was to investigate the potential for using nocturnal down-valley winds (cold air drainage) for monitoring ecosystem processes in mountainous terrain from two perspectives: measurements of the isotopic composition of ecosystem-respired CO2 (delta13C(ER)) and estimates of fluxes of CO2 transported in the drainage flow. To test if this approach is plausible, we monitored the wind patterns, CO2 concentrations, and the carbon isotopic composition of the air as it exited the base of a young (approximately 40 yr-old) and an old (>450 yr-old) steeply sided Douglas-fir watershed. Nocturnal cold air drainage within these watersheds was strong, deep, and occurred on more than 80% of summer nights. The depth of cold air drainage rapidly increased to tower height or greater when the net radiation at the top of the tower approached zero. The carbon isotope composition of CO2 in the drainage system holds promise as an indicator of variation in basin-scale physiological processes. Although there was little vertical variation in CO2 concentration at any point in time, we found that the range of CO2 concentration over a single evening was sufficient to estimate delta 13C(ER) from Keeling plot analyses. The seasonal variation in delta 13C(ER) followed expected trends: during the summer dry season delta 13C(ER) became less negative (more enriched in 13C), but once rain returned in the fall, delta 13C(ER) decreased. However, we found no correlation between recent weather (e.g., vapor pressure deficit) and delta 13C(ER) either concurrently or with up to a one-week lag. Preliminary estimates suggest that the nocturnal CO2 flux advecting past the 28-m tower is a rather small fraction (<20%) of the watershed-scale respiration. This study demonstrates that monitoring the isotopic composition and CO2 concentration of cold air drainage at the base of a watershed provides a new tool for quantifying ecosystem metabolism in mountainous ecosystems on the basin scale.

Thermal-dissipation sap flow sensors may not yield consistent sap-flux estimates over multiple years

Sap flow techniques, such as thermal dissipation, involve an empirically derived relationship between sap flux and the temperature differential between a heated thermocouple and a nearby reference thermocouple inserted into the sapwood. This relationship has been widely tested but mostly with newly installed sensors. Increasingly, sensors are used for extended periods. After several months, tree growth, wounding, or other changes in water flow path may impair sensor performance. To quantify changes in sensor performance over time, we installed 23 sensors (one per tree) in 16-year-old Douglas-fir [Pseudotsuga menziesii (Mirb.) Franco] and red alder (Alnus rubra Bong.) in the western Cascades of Oregon and measured daily average sap flux (Js) from April through July 2001 and 2002. We assumed the measurements from 2001 to be unimpaired and the response of Js to vapor pressure deficit (δ) to be consistent under the same edaphic conditions. Differences from this assumption were attributed to “temporal sampling errors.” During the study, soil moisture (θ), did not differ on similar calendar dates, yet the slope of Js versus δ decreased significantly in the second year. In 2002, Js in Douglas-fir was 45% less than in 2001; in red alder, 30% less. Variations in δ could not explain the differences. A correction for temporal sampling errors improved estimates of Js from sensors used for more than one season. Differences in temporal sampling errors between the two species reveal underlying causal mechanisms. Evidence is presented that cambial growth causes errors in Douglas-fir.

Perspectives on next‐generation technology for environmental sensor networks

Sensor networks promise to transform and expand environmental science. However, many technological difficulties must be overcome to achieve this potential. Partnerships of ecologists with computer scientists and engineers are critical in meeting these challenges. Technological issues include promoting innovation in new sensor design, incorporating power optimization schemes, integrating appropriate communication protocols, streamlining data management and access, using innovative graphic and statistical analyses, and enabling both scientists and the public to access the results. Multidisciplinary partnerships are making major contributions to technological advances, and we showcase examples of this exciting new technology, as well as new approaches for training researchers to make effective use of emerging tools.

Belowground interactions for water between trees and grasses in a temperate semiarid agroforestry system

A fundamental hypothesis of agroforestry is the complementary use of soil resources. However, productivity of many agroforestry systems has been lower than expected due to net competition for water, highlighting the need for a mechanistic understanding of belowground interactions. The goal of this study was to examine root–root interactions for water in a temperate semiarid agroforestry system, based on ponderosa pines and a Patagonian grass. The hypotheses were: (a) A greater proportion of water uptake by pines is from deeper soil layers when they are growing with grasses than when they are growing alone; (b) Growth of grasses is improved by the use of water hydraulically lifted by pines. We used stable isotopes of O to analyze water sources of plants, and we measured sapflow direction in pine roots and continuous soil water content with a very sensitive system. We also installed barriers to isolate the roots of a set of grasses from pine roots, in which we measured water status, relative growth and water sources, comparing to control plants. The results indicated that pines and grasses show some complementary in the use of soil water, and that pines in agroforestry systems use less shallow water than pines in monoculture. We found evidence of hydraulic lift, but contradicting results were obtained comparing growth and isotope results of the root isolation experiment. Therefore, we could not reject nor accept that grasses use water that is hydraulically lifted by the pines, or that this results in a positive effect on grass growth. This information may contribute to understand the complex and variable belowground interactions in temperate agroforestry.