Alexander W. Cheesman

Stable isotopes in leaf water of terrestrial plants

Leaf water contains naturally occurring stable isotopes of oxygen and hydrogen in abundances that vary spatially and temporally. When sufficiently understood, these can be harnessed for a wide range of applications. Here, we review the current state of knowledge of stable isotope enrichment of leaf water, and its relevance for isotopic signals incorporated into plant organic matter and atmospheric gases. Models describing evaporative enrichment of leaf water have become increasingly complex over time, reflecting enhanced spatial and temporal resolution. We recommend that practitioners choose a model with a level of complexity suited to their application, and provide guidance. At the same time, there exists some lingering uncertainty about the biophysical processes relevant to patterns of isotopic enrichment in leaf water. An important goal for future research is to link observed variations in isotopic composition to specific anatomical and physiological features of leaves that reflect differences in hydraulic design. New measurement techniques are developing rapidly, enabling determinations of both transpired and leaf water δ(18) O and δ(2) H to be made more easily and at higher temporal resolution than previously possible. We expect these technological advances to spur new developments in our understanding of patterns of stable isotope fractionation in leaf water.

Elevated night-time temperatures increase growth in seedlings of two tropical pioneer tree species

Increased night-time temperatures, through their influence on dark respiration, have been implicated as a reason behind decreasing growth rates in tropical trees in the face of contemporary climate change. Seedlings of two neo-tropical tree species (Ficus insipida and Ochroma pyramidale) were grown in controlled-environment chambers at a constant daytime temperature (33°C) and a range of increasing night-time temperatures (22, 25, 28, 31°C) for between 39 d and 54 d. Temperature regimes were selected to represent a realistic baseline condition for lowland Panama, and a rise in night-time temperatures far in excess of those predicted for Central America in the coming decades. Experiments were complemented by an outdoor open-top chamber study in which night-time temperatures were elevated by 2.4°C above ambient. Increasing night-time temperatures resulted in > 2-fold increase in biomass accumulation in growth-chamber studies despite an increase in leaf-level dark respiration. Similar trends were seen in open-top chambers, in which elevated night-time temperatures resulted in stimulation of growth. These findings challenge simplistic considerations of photosynthesis-directed growth, highlighting the role of temperature-dependent night-time processes, including respiration and leaf development as drivers of plant performance in the tropics.

Growth response and acclimation of CO2 exchange characteristics to elevated temperatures in tropical tree seedlings

Predictions of how tropical forests will respond to future climate change are constrained by the paucity of data on the performance of tropical species under elevated growth temperatures. In particular, little is known about the potential of tropical species to acclimate physiologically to future increases in temperature. Seedlings of 10 neo-tropical tree species from different functional groups were cultivated in controlled-environment chambers under four day/night temperature regimes between 30/22 °C and 39/31 °C. Under well-watered conditions, all species showed optimal growth at temperatures above those currently found in their native range. While non-pioneer species experienced catastrophic failure or a substantially reduced growth rate under the highest temperature regime employed (i.e. daily average of 35 °C), growth in three lowland pioneers showed only a marginal reduction. In a subsequent experiment, three species (Ficus insipida, Ormosia macrocalyx, and Ochroma pyramidale) were cultivated at two temperatures determined as sub- and superoptimal for growth, but which resulted in similar biomass accumulation despite a 6°C difference in growth temperature. Through reciprocal transfer and temperature adjustment, the role of thermal acclimation in photosynthesis and respiration was investigated. Acclimation potential varied among species, with two distinct patterns of respiration acclimation identified. The study highlights the role of both inherent temperature tolerance and thermal acclimation in determining the ability of tropical tree species to cope with enhanced temperatures.

Microwave extraction-isotope ratio infrared spectroscopy (ME-IRIS): a novel technique for rapid extraction and in-line analysis of δ18O and δ2H values of water in plants, soils and insects.

RATIONALE Traditionally, stable isotope analysis of plant and soil water has been a technically challenging, labour-intensive and time-consuming process. Here we describe a rapid single-step technique which combines Microwave Extraction with Isotope Ratio Infrared Spectroscopy (ME-IRIS). METHODS Plant, soil and insect water is extracted into a dry air stream by microwave irradiation within a sealed vessel. The water vapor thus produced is carried to a cooled condensation chamber, which controls the water vapor concentration and flow rate to the spectrometer. Integration of the isotope signals over the whole analytical cycle provides quantitative δ(18)O and δ(2) H values for the initial liquid water contained in the sample. Calibration is carried out by the analysis of water standards using the same apparatus. Analysis of leaf and soil water by cryogenic vacuum distillation and IRMS was used to validate the ME-IRIS data. RESULTS Comparison with data obtained by cryogenic distillation and IRMS shows that the new technique provides accurate water isotope data for leaves from a range of field-grown tropical plant species. However, two exotic nursery plants were found to suffer from spectral interferences from co-extracted organic compounds. The precision for extracted leaf, stem, soil and insect water was typically better than ±0.3 ‰ for δ(18)O and ±2 ‰ for δ(2) H values, and better than ±0.1 ‰ for δ(18)O and ±1 ‰ for δ(2) H values when analyzing water standards. The effects of sample size, microwave power and duration and sample-to-sample memory on isotope values were assessed. CONCLUSIONS ME-IRIS provides rapid and low-cost extraction and analysis of δ(18)O and δ(2) H values in plant, soil and insect water (≈10-15 min for samples yielding ≈ 0.3 mL of water). The technique can accommodate whole leaves of many plant species.

Thermal tolerance, net CO2 exchange and growth of a tropical tree species, Ficus insipida, cultivated at elevated daytime and nighttime temperatures

Global warming and associated increases in the frequency and amplitude of extreme weather events, such as heat waves, may adversely affect tropical rainforest plants via significantly increased tissue temperatures. In this study, the response to two temperature regimes was assessed in seedlings of the neotropical pioneer tree species, Ficus insipida. Plants were cultivated in growth chambers at strongly elevated daytime temperature (39°C), combined with either close to natural (22°C) or elevated (32°C) nighttime temperatures. Under both growth regimes, the critical temperature for irreversible leaf damage, determined by changes in chlorophyll a fluorescence, was approximately 51°C. This is comparable to values found in F. insipida growing under natural ambient conditions and indicates a limited potential for heat tolerance acclimation of this tropical forest tree species. Yet, under high nighttime temperature, growth was strongly enhanced, accompanied by increased rates of net photosynthetic CO2 uptake and diminished temperature dependence of leaf-level dark respiration, consistent with thermal acclimation of these key physiological parameters.

The benefits of recycling: how photosynthetic bark can increase drought tolerance

[Extract] Understanding the drought physiology of woody plants has become an increasingly important focus of plant science research in recent years, spurred on by concern about the potential for widespread tree mortality in response to drought stress caused by global warming (McDowell et al., 2008; Allen et al., 2010). However, there is one aspect of how woody plants cope with water deficits that has received very little attention: the role of carbon fixation by photosynthetic bark. This process may become especially important for maintaining physiological activity in woody tissues of drought-stressed trees as the supply of photosynthate from leaves dwindles, due to stomatal closure and impaired phloem translocation. In this issue of New Phytologist, Vandegehuchte et al. (pp. 998–1002) bring this process into the spotlight, and provide a compelling argument for why we should take more notice of that often-hidden, green layer of tissue that is ubiquitous beneath the smooth-bark surfaces of woody plants (Scott, 1907; Pfanz et al., 2002; Dima et al., 2006; Rosell et al., 2015).

The role of topography and plant functional traits in determining tropical reforestation success

1. Early establishment and sapling growth is a key phase in ensuring cost-effective reforestation success in relation to biodiversity outcomes. Therefore species selection must consider the interaction between plant functional traits and the often-challenging and heterogeneous biophysical environment of degraded landscapes. 2. In this study, we examine how microtopography (slope) results in spatial heterogeneity of soil nutrients, especially phosphorus (P) in a degraded tropical pasture landscape in Queensland, Australia. We then explore how this small-scale heterogeneity influences the growth of two native tree species, Cardwellia (C.) sublimis (Proteaceae) and Flindersia (F.) brayleyana (Rutaceae), which differ in key nutrient-acquisition strategies. 3. The proteaceous C. sublimis was found to be buffered from possible P limitation in degraded soils due to its effective P acquisition by cluster roots. In contrast to C. sublimis, which showed no difference in growth after 5 years across a range of soil conditions, F. brayleyana was found to be highly responsive to soil conditions with increased growth in low-slope, higher P availability areas. The ability of F. brayleyana to take advantage of high soil P levels, including the development of leaves with higher P concentrations, resulted in an apparent switch in competitive fitness between these two species across a landscape gradient. 4. Synthesis and applications. In a detailed study of a landscape reforestation experiment in North Queensland, Australia, we demonstrate that site edaphic factors can vary within tens of meters due to topographic relief, and that species respond differently to these conditions. We therefore show the need to consider both the spatial heterogeneity of edaphic factors and the below ground functional traits of potential reforestation species when planning reforestation programs.

Plant functional groups within a tropical forest exhibit different wood functional anatomy

Summary Understanding the anatomical basis of plant water transport in forest ecosystems is crucial for contextualizing community-level adaptations to drought, especially in life-form-rich tropical forests. To provide this context, we explored wood functional anatomy traits related to plant hydraulic architecture across different plant functional groups in a lowland tropical rain forest. We measured wood traits in 90 species from six functional groups (mature-phase, understorey and pioneer trees; understorey and pioneer shrubs; vines) and related these traits to intrinsic water-use efficiency (WUEi) as a measure of physiological performance. We also examined vessel size distribution patterns across groups to determine trade-offs in theoretical hydraulic safety vs. efficiency. Some plant functional groups exhibited significant differences in vessel parameters and WUEi. Vessel diameters in vines and pioneer trees were two- to threefold greater on average than in understorey trees and shrubs. Contrastingly, vessels in understorey trees and shrubs fell within the smaller size classes, suggesting greater safety mechanisms. In addition to these trends, large vessel dimensions were important predictors of WUEi among the functional groups. We conclude that wood functional anatomy profiles varied across plant functional groups in a tropical rain forest. These groups can therefore serve as a framework for further investigations on structure–function relationships and a sound basis for modelling species responses to drought. A lay summary is available for this article.

Current ambient concentrations of ozone in Panama modulate the leaf chemistry of the tropical tree Ficus insipida

Tropospheric ozone (O3) is a major air pollutant and greenhouse gas, affecting carbon dynamics, ecological interactions, and agricultural productivity across continents and biomes. Elevated [O3] has been documented in tropical evergreen forests, the epicenters of terrestrial primary productivity and plant-consumer interactions. However, the effects of O3 on vegetation have not previously been studied in these forests. In this study, we quantified ambient O3 in a region shared by forests and urban/commercial zones in Panama and found levels two to three times greater than in remote tropical sites. We examined the effects of these ambient O3 levels on the growth and chemistry of seedlings of Ficus insipida, a regionally widespread tree with high stomatal conductance, using open-top chambers supplied with ozone-free or ambient air. We evaluated the differences across treatments in biomass and, using UPLC-MS-MS, leaf secondary metabolites and membrane lipids. Mean [O3] in ambient air was below the levels that induce chronic stress in temperate broadleaved trees, and biomass did not differ across treatments. However, leaf secondary metabolites - including phenolics and a terpenoid - were significantly downregulated in the ambient air treatment. Membrane lipids were present at lower concentrations in older leaves grown in ambient air, suggesting accelerated senescence. Thus, in a tree species with high O3 uptake via high stomatal conductance, current ambient [O3] in Panamanian forests are sufficient to induce chronic effects on leaf chemistry.