Amy E. Zanne

Towards a worldwide wood economics spectrum

Wood performs several essential functions in plants, including mechanically supporting aboveground tissue, storing water and other resources, and transporting sap. Woody tissues are likely to face physiological, structural and defensive trade-offs. How a plant optimizes among these competing functions can have major ecological implications, which have been under-appreciated by ecologists compared to the focus they have given to leaf function. To draw together our current understanding of wood function, we identify and collate data on the major wood functional traits, including the largest wood density database to date (8412 taxa), mechanical strength measures and anatomical features, as well as clade-specific features such as secondary chemistry. We then show how wood traits are related to one another, highlighting functional trade-offs, and to ecological and demographic plant features (growth form, growth rate, latitude, ecological setting). We suggest that, similar to the manifold that tree species leaf traits cluster around the leaf economics spectrum, a similar wood economics spectrum may be defined. We then discuss the biogeography, evolution and biogeochemistry of the spectrum, and conclude by pointing out the major gaps in our current knowledge of wood functional traits.

Functional traits and the growth?mortality trade-off in tropical trees

A trade-off between growth and mortality rates characterizes tree species in closed canopy forests. This trade-off is maintained by inherent differences among species and spatial variation in light availability caused by canopy-opening disturbances. We evaluated conditions under which the trade-off is expressed and relationships with four key functional traits for 103 tree species from Barro Colorado Island, Panama. The trade-off is strongest for saplings for growth rates of the fastest growing individuals and mortality rates of the slowest growing individuals (r2 = 0.69), intermediate for saplings for average growth rates and overall mortality rates (r2 = 0.46), and much weaker for large trees (r2 < or = 0.10). This parallels likely levels of spatial variation in light availability, which is greatest for fast- vs. slow-growing saplings and least for large trees with foliage in the forest canopy. Inherent attributes of species contributing to the trade-off include abilities to disperse, acquire resources, grow rapidly, and tolerate shade and other stresses. There is growing interest in the possibility that functional traits might provide insight into such ecological differences and a growing consensus that seed mass (SM), leaf mass per area (LMA), wood density (WD), and maximum height (H(max)) are key traits among forest trees. Seed mass, LMA, WD, and H(max) are predicted to be small for light-demanding species with rapid growth and mortality and large for shade-tolerant species with slow growth and mortality. Six of these trait-demographic rate predictions were realized for saplings; however, with the exception of WD, the relationships were weak (r2 < 0.1 for three and r2 < 0.2 for five of the six remaining relationships). The four traits together explained 43-44% of interspecific variation in species positions on the growth-mortality trade-off; however, WD alone accounted for > 80% of the explained variation and, after WD was included, LMA and H(max) made insignificant contributions. Virtually the full range of values of SM, LMA, and H(max) occurred at all positions on the growth-mortality trade-off. Although WD provides a promising start, a successful trait-based ecology of tropical forest trees will require consideration of additional traits.

Global meta-analysis of wood decomposition rates: a role for trait variation among tree species?

The carbon flux from woody debris, a crucial uncertainty within global carbon-climate models, is simultaneously affected by climate, site environment and species-based variation in wood quality. In the first global analysis attempting to explicitly tease out the wood quality contribution to decomposition, we found support for our hypothesis that, under a common climate, interspecific differences in wood traits affect woody debris decomposition patterns. A meta-analysis of 36 studies from all forested continents revealed that nitrogen, phosphorus, and C : N ratio correlate with decomposition rates of angiosperms. In addition, gymnosperm wood consistently decomposes slower than angiosperm wood within common sites, a pattern that correlates with clear divergence in wood traits between the two groups. New empirical studies are needed to test whether this difference is due to a direct effect of wood trait variation on decomposer activity or an indirect effect of wood traits on decomposition microsite environment. The wood trait-decomposition results point to an important role for changes in the wood traits of dominant tree species as a driver of carbon cycling, with likely feedback to atmospheric CO(2) particularly where angiosperm species replace gymnosperms regionally. Truly worldwide upscaling of our results will require further site-based multi-species wood trait and decomposition data, particularly from low-latitude ecosystems.

Angiosperm wood structure: Global patterns in vessel anatomy and their relation to wood density and potential conductivity

Woody stems comprise a large biological carbon fraction and determine water transport between roots and leaves; their structure and function can influence both carbon and hydrological cycles. While angiosperm wood anatomy and density determine hydraulic conductivity and mechanical strength, little is known about interrelations across many species. We compiled a global data set comprising two anatomical traits for 3005 woody angiosperms: mean vessel lumen area (Ā) and number per unit area (N). From these, we calculated vessel lumen fraction (F = ĀN) and size to number ratio (S = Ā/N), a new vessel composition index. We examined the extent to which F and S influenced potential sapwood specific stem conductivity (K(S)) and wood density (D; dry mass/fresh volume). F and S varied essentially independently across angiosperms. Variation in K(S) was driven primarily by S, and variation in D was virtually unrelated to F and S. Tissue density outside vessel lumens (D(N)) must predominantly influence D. High S should confer faster K(S) but incur greater freeze-thaw embolism risk. F should also affect K(S), and both F and D(N) should influence mechanical strength, capacitance, and construction costs. Improved theory and quantification are needed to better understand ecological costs and benefits of these three distinct dimensions.

On research priorities to advance understanding of the safety-efficiency tradeoff in xylem: A response to Bittencourt et al.'s (2016) comment 'On xylem hydraulic efficiencies, wood space-use and the safety-efficiency tradeoff': in this issue of New Phytologist, pp. 1152-1155

We appreciate Bittencourt et al.’s (2016) constructive contributions following our paper, Gleason et al. (2016), on the proposed tradeoff between hydraulic safety and efficiency. To continue this dialog we would like to comment on which of the research directions proposed by Bittencourt et al. seem most promising to us. We agree that various xylem tissue fractions could potentially modify the safety–efficiency relationship. In principle, any tissue fraction could trade off with any other tissue fraction. However, as a matter of observation, parenchyma fraction is negatively correlated with fiber fraction, whereas parenchyma and fiber fractions are not strongly correlated with vessel lumen fraction (Ziemi! nska et al., 2015; Morris et al., 2016). As such, vessel lumen fraction, vessel diameter, and vessel frequency are largely uncoupled from nonvessel tissue fractions across self-supporting angiosperm species (Zanne et al., 2010), and are therefore unlikely to trade off with mechanical safety and hydraulic efficiency (or safety). Furthermore, vessel lumen fraction itself does not vary markedly across angiosperms, ranging from c. 5% to 20% (mean! 15%) (Zanne et al., 2010; Morris et al., 2016), although larger fractions are not uncommon in ring-porous and climbing species. Contrasts between climbing (e.g. lianas) and freestanding growth forms are more likely to show differences in allocation to vessel vs nonvessel space, and the climbing habit therefore may offer a more appropriate system for evaluating this idea (Gartner, 1991). Gymnosperm xylem differs from angiosperm xylem in that it generally lacks axial parenchyma, and conduits are both conductive and load-bearing. Greater mechanical safety may be negatively correlated with both hydraulic safety and efficiency across gymnosperm species (Mayr & Cochard, 2003; Mayr et al., 2003). Considering angiosperms, it is likely that nonvessel tissue fractions influence the safety–efficiency tradeoff indirectly (e.g. via their contribution to xylem capacitance, or whole-plant growth), rather than being forced by limited xylem space. Bittencourt et al. suggest that expressing conductivity as a ratio with mass, rather than cross-sectional area, might better characterize the energetic costs associated with xylem. We agree with this suggestion and did consider the influence of specific gravity on the safety–efficiency tradeoff in our paper (Table 2 and Figs 3d, 4d in Gleason et al., 2016). Here, we formulate these results by expressing the y axis explicitly as xylem-specific conductivity/ specific gravity (Fig. 1), as suggested by Bittencourt et al. Specific gravity, safety and efficiency values were generally obtained from the same published reports. Similar to the results we report in Gleason et al. (2016), including specific gravity in the analyses increases the tradeoff r 2 in both angiosperms (0.11–0.14) and gymnosperms (0.10–0.15) when safety is defined as P50. A similar increase in r 2 is achieved when defining safety as P88 and there is no change when defining safety as P12. Although including xylem density does increase the amount of variation explained by the models, they still fall far short of explaining why many species exhibit both low safety and low efficiency. Despite the analysis provided in Fig. 1, we feel that the clearest approach to analyzing these inter-correlated variables will be to consider all known sources of variation (e.g. structural equation models) rather than expressing them as a ratio with conductivity (e.g. conductivity/parenchyma fraction). Such ratios build an assumption of proportionality between the two elements of the ratio, which are not necessarily what we should expect. It remains a possibility that xylem safety, expressed as the xylem water potential at which a fraction of maximal conductance is lost, may not be an accurate approximation for all species in all situations. Although we agree in principle that safety (e.g. P50) may not correlate with mortality similarly across species, there is good evidence to suggest that it does for many angiosperm and gymnosperm species (Pratt et al., 2008; Brodribb & Cochard, 2009; Brodribb et al., 2010). This suggests that there may be an intrinsic property of xylem to resist desiccation (angiosperm Ψleaf > P88; gymnosperm Ψleaf > P50), beyond which the probability of mortality increases precipitously. Measurements of hydraulic safety, as well as conductivity during drought, should serve as more appropriate predictors of mortality than other measurements of water status (e.g. turgor loss point in leaves or stomatal response) because percentage loss of conductance is a meaningful representation of xylem desiccation. However, it is also clear that there are mechanisms that delay the time to reach a desiccation–mortality threshold. As suggested by Bittencourt et al. and Brodersen (2016), these would include deciduousness, deep rooting, reduced stomatal ‘leakiness’, reduced cuticular conductance, CAM and C4 metabolism, and capacitance. However, considering tradeoffs with either safety or efficiency, in isolation of one another (e.g. safety–capacitance), does not inform our efforts to understand the proposed link between safety and efficiency. For example, if greater capacitance reduces the requirement for safety, natural selection should still be free to improve efficiency, which would provide benefit via greater