Frida I. Piper

Intraspecific trait variation and covariation in a widespread tree species (Nothofagus pumilio) in southern Chile

• The focus of the trait-based approach to study community ecology has mostly been on trait comparisons at the interspecific level. Here we quantified intraspecific variation and covariation of leaf mass per area (LMA) and wood density (WD) in monospecific forests of the widespread tree species Nothofagus pumilio to determine its magnitude and whether it is related to environmental conditions and ontogeny. We also discuss probable mechanisms controlling the trait variation found. • We collected leaf and stem woody tissues from 30-50 trees of different ages (ontogeny) from each of four populations at differing elevations (i.e. temperatures) and placed at each of three locations differing in soil moisture. • The total variation in LMA (coefficient of variation (CV) = 21.14%) was twice that of WD (CV = 10.52%). The total variation in traits was never less than 23% when compared with interspecific studies. Differences in elevation (temperature) for the most part explained variation in LMA, while differences in soil moisture and ontogeny explained the variation in WD. Traits covaried similarly in the altitudinal gradient only. • Functional traits of N. pumilio exhibited nonnegligible variation; LMA varied for the most part with temperature, while WD mostly varied with moisture and ontogeny. We demonstrate that environmental variation can cause important trait variation without species turnover.

Non-structural carbohydrates in woody plants compared among laboratories

Non-structural carbohydrates (NSC) in plant tissue are frequently quantified to make inferences about plant responses to environmental conditions. Laboratories publishing estimates of NSC of woody plants use many different methods to evaluate NSC. We asked whether NSC estimates in the recent literature could be quantitatively compared among studies. We also asked whether any differences among laboratories were related to the extraction and quantification methods used to determine starch and sugar concentrations. These questions were addressed by sending sub-samples collected from five woody plant tissues, which varied in NSC content and chemical composition, to 29 laboratories. Each laboratory analyzed the samples with their laboratory-specific protocols, based on recent publications, to determine concentrations of soluble sugars, starch and their sum, total NSC. Laboratory estimates differed substantially for all samples. For example, estimates for Eucalyptus globulus leaves (EGL) varied from 23 to 116 (mean = 56) mg g(-1) for soluble sugars, 6-533 (mean = 94) mg g(-1) for starch and 53-649 (mean = 153) mg g(-1) for total NSC. Mixed model analysis of variance showed that much of the variability among laboratories was unrelated to the categories we used for extraction and quantification methods (method category R(2) = 0.05-0.12 for soluble sugars, 0.10-0.33 for starch and 0.01-0.09 for total NSC). For EGL, the difference between the highest and lowest least squares means for categories in the mixed model analysis was 33 mg g(-1) for total NSC, compared with the range of laboratory estimates of 596 mg g(-1). Laboratories were reasonably consistent in their ranks of estimates among tissues for starch (r = 0.41-0.91), but less so for total NSC (r = 0.45-0.84) and soluble sugars (r = 0.11-0.83). Our results show that NSC estimates for woody plant tissues cannot be compared among laboratories. The relative changes in NSC between treatments measured within a laboratory may be comparable within and between laboratories, especially for starch. To obtain comparable NSC estimates, we suggest that users can either adopt the reference method given in this publication, or report estimates for a portion of samples using the reference method, and report estimates for a standard reference material. Researchers interested in NSC estimates should work to identify and adopt standard methods.

A multi-species synthesis of physiological mechanisms in drought-induced tree mortality

Widespread tree mortality associated with drought has been observed on all forested continents and global change is expected to exacerbate vegetation vulnerability. Forest mortality has implications for future biosphere–atmosphere interactions of carbon, water and energy balance, and is poorly represented in dynamic vegetation models. Reducing uncertainty requires improved mortality projections founded on robust physiological processes. However, the proposed mechanisms of drought-induced mortality, including hydraulic failure and carbon starvation, are unresolved. A growing number of empirical studies have investigated these mechanisms, but data have not been consistently analysed across species and biomes using a standardized physiological framework. Here, we show that xylem hydraulic failure was ubiquitous across multiple tree taxa at drought-induced mortality. All species assessed had 60% or higher loss of xylem hydraulic conductivity, consistent with proposed theoretical and modelled survival thresholds. We found diverse responses in non-structural carbohydrate reserves at mortality, indicating that evidence supporting carbon starvation was not universal. Reduced non-structural carbohydrates were more common for gymnosperms than angiosperms, associated with xylem hydraulic vulnerability, and may have a role in reducing hydraulic function. Our finding that hydraulic failure at drought-induced mortality was persistent across species indicates that substantial improvement in vegetation modelling can be achieved using thresholds in hydraulic function.The mechanisms underlying drought-induced tree mortality are not fully resolved. Here, the authors show that, across multiple tree species, loss of xylem conductivity above 60% is associated with mortality, while carbon starvation is not universal.

Drought induces opposite changes in the concentration of non-structural carbohydrates of two evergreen Nothofagus species of differential drought resistance

Abstract• IntroductionOne current explanation for worldwide drought-induced tree mortality states that reduced photosynthesis and continued respiration lead to carbon depletion and eventually to carbon starvation.• MethodsTo determine if variations in gas exchange are consistent with variations in carbon storage, and if such consistency may depend on the drought resistance of a species, I examined the non-structural carbohydrates (NSC) concentration and gas exchange in seedlings of two Nothofagus species of differential drought resistance under severe drought—just before death—and under well-watered conditions.• Results and discussionDrought provoked decreased photosynthesis and had no effect on leaf respiration in both species, whereas NSC concentrations varied oppositely: it decreased in the relatively more drought-susceptible species (Nothofagus nitida) whilst it increased in the relatively more drought-resistant species (Nothofagus dombeyi). Thus, if carbon balance would have been inferred from gas exchange alone, I would have wrongly concluded that carbon depletion occurred in both species. In stressed seedlings of N. nitida, photosynthesis and NSC concentrations were negatively correlated in roots (r2 = −0.57, p = 0.03) and not correlated in stems (r2 = −0.05, p = 0.58), indicating that carbon depletion due to reduced photosynthesis was not occurring at harvest time, but it took place earlier when water stress was milder.• ConclusionsResults demonstrate that carbon depletion cannot be predicted from measurements of gas exchange. Drought-induced mobilization of carbon storage appeared influenced by the drought resistance of the species and by drought intensity.

Variation of mobile carbon reserves in trees at the alpine treeline ecotone is under environmental control

In low temperature-adapted plants, including treeline trees, light-saturated photosynthesis is considerably less sensitive to temperature than growth. As a consequence, all plants tested so far show increased nonstructural carbohydrate (NSC) tissue concentrations when exposed to low temperatures. Reduced carbon supply is thus an unlikely cause for low temperature range limits of plants. For altitudinal treeline trees there is, however, a possibility that high NSC genotypes have been selected. Here, we explored this possibility using afforestations with single-provenance conifers along elevational gradients in the Southern Chilean Andes and the Swiss Alps. Tree growth was measured at each of four approximately equidistant elevations at and below the treeline. Additionally, at the same elevations, needle, branch and stem sapwood tissues were collected to determine NSC concentrations. Overall, growth decreased and NSC concentrations increased with elevation. Along with previous empirical and experimental studies, the findings of this study provide no indication of NSC reduction at the treeline; NSC increased in most species (each represented by one common population) towards their upper climatic limit. The disparity between carbon acquisition and structural carbon investment at low temperature (accumulation of NSC) thus does occur even among genotypes not adapted to treeline environments.

Similar variation in carbon storage between deciduous and evergreen treeline species across elevational gradients

BACKGROUND AND AIMS The most plausible explanation for treeline formation so far is provided by the growth limitation hypothesis (GLH), which proposes that carbon sinks are more restricted by low temperatures than by carbon sources. Evidence supporting the GLH has been strong in evergreen, but less and weaker in deciduous treeline species. Here a test is made of the GLH in deciduous-evergreen mixed species forests across elevational gradients, with the hypothesis that deciduous treeline species show a different carbon storage trend from that shown by evergreen species across elevations. METHODS Tree growth and concentrations of non-structural carbohydrates (NSCs) in foliage, branch sapwood and stem sapwood tissues were measured at four elevations in six deciduous-evergreen treeline ecotones (including treeline) in the southern Andes of Chile (40°S, Nothofagus pumilio and Nothofagus betuloides; 46°S, Nothofagus pumilio and Pinus sylvestris) and in the Swiss Alps (46°N, Larix decidua and Pinus cembra). KEY RESULTS Tree growth (basal area increment) decreased with elevation for all species. Regardless of foliar habit, NSCs did not deplete across elevations, indicating no shortage of carbon storage in any of the investigated tissues. Rather, NSCs increased significantly with elevation in leaves (P < 0·001) and branch sapwood (P = 0·012) tissues. Deciduous species showed significantly higher NSCs than evergreens for all tissues; on average, the former had 11 % (leaves), 158 % (branch) and 103 % (sapwood) significantly (P < 0·001) higher NSCs than the latter. Finally, deciduous species had higher NSC (particularly starch) increases with elevation than evergreens for stem sapwood, but the opposite was true for leaves and branch sapwood. CONCLUSIONS Considering the observed decrease in tree growth and increase in NSCs with elevation, it is concluded that both deciduous and evergreen treeline species are sink limited when faced with decreasing temperatures. Despite the overall higher requirements of deciduous tree species for carbon storage, no indication was found of carbon limitation in deciduous species in the alpine treeline ecotone.

Carbohydrate storage, survival, and growth of two evergreen Nothofagus species in two contrasting light environments

A number of traits have been attributed important roles in tolerance of shade by plants. Some explanations emphasize traits enhancing net carbon gain; others emphasize energy conservation traits such as storage of non-structural carbohydrates (NSC). To date, cross-species studies have provided mixed support for the role of NSC storage in low-light survival. We examined NSC status, survival, biomass, and growth of large seedlings of two evergreen species of differing shade tolerance (Nothofagus nitida and N. dombeyi) grown in deep shade and 50% light for two growing seasons. We expected to find higher NSC concentration in the more shade-tolerant N. nitida and since allocation to storage involves sacrificing growth, higher growth rate in the shade-intolerant N. dombeyi. NSC concentration of both species was >twofold higher in 50% light than in deep shade, and in roots and stems did not differ significantly between species in either environment. NSC contents per plant were also similar between dead and living plants in deep shade. N. dombeyi outgrew N. nitida in 50% light, while this pattern was reversed in deep shade. Survival in deep shade was not correlated with NSC concentration. Leaf mass fraction was similar between species in 50% light, but lower in N. dombeyi in deep shade. Results provide little evidence of a link between carbohydrate storage and low-light survival in Nothofagus species, and support the view that understorey survival is primarily a function of net carbon gain. Patterns of variation in NSC concentration of the temperate species we studied are likely dominated by more important influences than adaptation to shade, such as limitation of growth or adaptation to cold stress.

Differential photosynthetic and survival responses to soil drought in two evergreen Nothofagus species

We asked if differences in distribution between Nothofagus nitida and N. dombeyi were associated with differences in drought tolerance. Survival, gas exchange and chlorophyll fluorescence were measured on seedlings subjected to a gradual drought. At a predawn leaf water potential (Ψm) of −2.7 MPa, survival of N. nitida was 50%, compared to 100% in N. dombeyi. Under well-watered conditions, the two species displayed similar stomatal conductance (gw) and transpiration (E), but net photosynthesis (A) and instantaneous water-use efficiency (WUEi) were slightly higher in N. nitida. A, E and gw declined in N. nitida along the gradual drought but increased in N. dombeyi at a Ψm between −1.5 and −2.5 MPa, and declined then drastically at a Ψm below < −2.5 MPa. As N. dombeyi was able to maintain A at higher levels despite declining gw, this species displayed significantly increased WUEi at Ψm below −2.5 MPa. Photochemical efficiency of PSII in the light (ΔF/Fmr) and photochemical quenching (qP) were always lower in N. nitida and along with the photochemical efficiency in the dark (Fv/Fm) they declined in both species. Non-photochemical quenching (NPQ) increased slowly in N. dombeyi along with the gradual drought, whilst it decreased in N. nitida. These results show that differences in drought tolerance are in agreement with sorting of Nothofagus species along moisture gradients in south-central Chile.RésuméNous nous sommes demandés si des différences de distribution entre Nothofagus nitida et N. dombeyi sont associées à des différences de tolérance à la sécheresse. La survie, les échanges gazeux et la fluorescence de la chlorophylle ont été mesurés sur de jeunes plants soumis à une sécheresse croissante. Lorsque le potentiel hydrique de base (Ψm) atteignait −2.7 MPa la survie était de 50 et de 100 % pour N. nitida, et N. dombeyi, respectivement. Dans des conditions d’alimentation hydrique suffisante, les deux espèces ont présenté des valeurs voisines de conductance stomatique (gw) et de transpiration (E) mais la photosynthèse nette (A) et l’effitience instantanée d’utilisation de l’eau (WUEi) étaient légèrement plus élevées pour N. nitida. A, E et gw ont diminué pour N. nitida au cours d’une sécheresse croissante mais ont légèrement augmenté pour N. dombeyi pour des valeurs de Ψm comprises entre −1.5 et −2.5 MPa, puis diminué fortement à des valeurs de Ψm inférieures à −2.5 MPa. Par conséquent, N. dombeyi a présenté des valeurs de WUEi plus élevée que N. nitida à des niveaux de Ψm inferieurs à −2.5 MPa. L’effitience photochimique du PSII à la lumière (ΔF/Fm) et le quenching photochimique (qp) étaient toujours inférieurs pour N. nitida. L’effitience photochimique à l’obscurité (Fv/Fm) ainsi que ΔFjFm ont diminué dans les deux espèces. Le quenching non-photochimique (NPQ) a légèrement augmenté pour N. dombeyi avec la sécheresse, alors qu’il diminuait pour N. nitida. Ces résultats montrent que des différences de tolérance à la sécheresse correspondent à la distribution d’espèces de Nothofagus le long de gradients d’humidité dans le centre sud du Chili.

Ontogeny, understorey light interception and simulated carbon gain of juvenile rainforest evergreens differing in shade tolerance

BACKGROUND AND AIMS A long-running debate centres on whether shade tolerance of tree seedlings is mainly a function of traits maximizing net carbon gain in low light, or of traits minimizing carbon loss. To test these alternatives, leaf display, light-interception efficiency, and simulated net daily carbon gain of juvenile temperate evergreens of differing shade tolerance were measured, and how these variables are influenced by ontogeny was queried. METHODS The biomass distribution of juveniles (17-740 mm tall) of seven temperate rainforest evergreens growing in low (approx. 4 %) light in the understorey of a second-growth stand was quantified. Daytime and night-time gas exchange rates of leaves were also determined, and crown architecture was recorded digitally. YPLANT was used to model light interception and carbon gain. RESULTS An index of species shade tolerance correlated closely with photosynthetic capacities and respiration rates per unit mass of leaves, but only weakly with respiration per unit area. Accumulation of many leaf cohorts by shade-tolerant species meant that their ratios of foliage area to biomass (LAR) decreased more gradually with ontogeny than those of light-demanders, but also increased self-shading; this depressed the foliage silhouette-to-area ratio (STAR), which was used as an index of light-interception efficiency. As a result, displayed leaf area ratio (LAR(d) = LAR × STAR) of large seedlings was not related to species shade tolerance. Self-shading also caused simulated net daily carbon assimilation rates of shade-tolerant species to decrease with ontogeny, leading to a negative correlation of shade tolerance with net daily carbon gain of large (500 mm tall) seedlings in the understorey. CONCLUSIONS The results suggest that efficiency of energy capture is not an important correlate of shade tolerance in temperate rainforest evergreens. Ontogenetic increases in self-shading largely nullify the potential carbon gain advantages expected to result from low respiration rates and long leaf lifespans in shade-tolerant evergreens. The main advantage of their long-lived leaves is probably in reducing the costs of crown maintenance.

An experimental approach to explain the southern Andes elevational treeline

UNLABELLED • PREMISE OF THE STUDY The growth limitation hypothesis (GLH) is the most accepted mechanistic explanation for treeline formation, although it is still uncertain whether it applies across taxa. The successful establishment of Pinus contorta--an exotic conifer species in the southern hemisphere--above the Nothofagus treeline in New Zealand may suggest a different mechanism. We tested the GLH in Nothofagus pumilio and Pinus contorta by comparing seedling performance and carbon (C) balance in response to low temperatures.• METHODS At a southern Chilean treeline, we grew seedlings of both species 2 m above ground level, to simulate coupling between temperatures at the meristem and in the air (colder), and at ground level, i.e., decoupling air temperature (relatively milder). We recorded soil and air temperatures as well. After 3 yr, we measured seedling survival and biomass (as a surrogate of growth) and determined nonstructural carbohydrates (NSC).• KEY RESULTS Nothofagus and Pinus did not differ in survival, which, as a whole, was higher at ground level than at the 2-m height. The root-zone temperature for the growing season was 6.6°C. While biomass and NSC decreased significantly for Nothofagus at the 2-m height compared with ground level (C limitation), these trends were not significant for Pinus• CONCLUSIONS The treeline for Nothofagus pumilio is located at an isotherm that fully matches global patterns; however, its physiological responses to low temperatures differed from those of other treeline species. Support for C limitation in N. pumilio but not in P. contorta indicates that the physiological mechanism explaining their survival and growth at treeline may be taxon-dependent.