Tree Physiology Advance Access published November 23, 2016

Tree Physiology 00, 1–3 doi:10.1093/treephys/tpw111

Commentary

Bridging long-term wood functioning and nitrogen deposition to better understand changes in tree growth and forest productivity J. Julio Camarero1,3 and Marco Carrer2 1

Instituto Pirenaico de Ecología (IPE-CSIC), Avda Montañana 1005, Zaragoza 50059, Spain; 2Dip. TeSAF, Universitá degli Studi di Padova, Agripolis, I-35020 Legnaro, Italy; Corresponding author ([email protected])

Received September 22, 2016; accepted November 2, 2016; handling Editor Danielle Way

The global nitrogen cycle and functional wood ecology The worldwide increase in nitrogen (N) deposition due to the burning of fossil fuels and the extensive use of fertilizers represents one of the major facets of current global change (Galloway et al. 2008). Increased rates of N deposition are typically expected to enhance forest productivity and tree growth (Gruber and Galloway 2008). However, the long-term consequences of this form of N fertilization on tree functioning are still mostly unclear (Vitousek et al. 1997). Furthermore, tree growth and wood formation can also be affected by climate warming and the rise in atmospheric CO2 concentrations (ca). While radial growth, which should increase under increasing N availability, is tightly linked to wood-anatomical traits and hydraulic conductivity, we still lack approaches bridging long-term N deposition patterns and changes in hydraulic architecture (but see Ewers et al. 2000, Hacke et al. 2010). As happened with functional leaf traits associated with the leaf economics spectrum (Wright et al. 2004), to date wood functional traits have been receiving increasingly more attention in our efforts to understand tree functioning (Reich et al. 1992, Chave et al. 2009, Zanne et al. 2010, Hietz et al. 2016). Leaf N content is directly correlated with the protein concentrations responsible for photosynthesis and also influences carbon (C) allocation, respiration and growth rates. However, the lack of mechanistic models linking N dynamics and wood traits, together with the very timeconsuming effort required to retrieve well-replicated and robust wood-anatomical records, could explain the relative scarcity of longterm studies on functional wood traits as related to increasing N deposition. In this issue of Tree Physiology, Borghetti et al. (2016)

aim to fill this research gap by assessing how variability in environmental drivers, such as climate and N deposition rates, is related to wood traits such as growth rate (tree-ring width) and xylem anatomy (mainly conduit area and conduit density). With a meta-analysis approach, Borghetti et al. (2016) investigated how N deposition related to xylem traits across a wide assemblage of environmental conditions and species. They did not detect any pervasive long-term trends in the tree-ring width series potentially consistent with the CO2-related fertilization effect on growth. In addition, conduit size and density were not negatively associated in their data set, arguing against the existence of a trade-off between these two traits, as was also reported by Gleason et al. (2015). But the authors did find that increasing N deposition might be linked to improved hydraulic efficiency in xylem due to enhanced conduit density. A previous analysis by the same group also found a relationship between the cumulative N deposition rate and the increase in intrinsic water-use efficiency (iWUE) (Leonardi et al. 2012). These two studies represent promising efforts given the cited difficulty in dealing with long-term quantitative woodanatomy data, and linking them with N deposition rates. The work of Borghetti et al. (2016) provides an important step forward, but to fully bridge wood functional traits with N dynamics, several caveats should be thoroughly considered. The first concerns whether we can use the conceptual framework developed for tree nutrition to understand N deposition effects on hydraulic architecture. Since N deposition involves changes in a large suite of environmental (soil acidification, nutrient imbalances, nutrient toxicity) and biological (plant respiration and C allocation patterns) processes, it is possible that purely

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2 Camarero and Carrer

The other way around: reconstructing the nitrogen cycle from wood Long-term records of tree-ring data and xylem anatomical traits have allowed the effects of temperatures or drought on growth

Tree Physiology Volume 00, 2016

rates, conduit lumen dimension, kinetics of tracheid development and vessel patterning to be uncovered (Vaganov et al. 2006, Fonti et al. 2010, Anderegg et al. 2015). Long-term changes in iWUE have also been inferred by studying C isotopes in tree-ring wood and cellulose (McCarroll and Loader 2004, Saurer et al. 2004). Nevertheless, addressing the long-term influences of increased N deposition on forest productivity and tree functioning is a challenge for several reasons. For instance, N concentrations in woody tissues are usually low, ranging from 0.04% to 0.59%, and highly variable among taxonomic groups and tissues (Meerts 2002, Martin et al. 2014, 2015). This variability between tissues is not trivial since the N diminution from sapwood to heartwood has been associated with a higher resistance to fungi degradation (Merrill and Cowling 1966). It has been argued that long-term assessments of the impact of increasingly available N on forest productivity could be studied by retrospectively analyzing stable nitrogen isotope analysis (15N/14N, δ15N) in tree-ring series (Gerhart and McLauchlan 2014). This is a promising research avenue: studies conducted in tropical forests and using wood chronologies suggest an increase in N availability due to the effect of anthropogenic N deposition rates (Hietz et al. 2010, 2011). Alas, a retrospective inference of N availability to trees based on xylem variables may not be so simple since protocol details are still unclear (N can be translocated between living sapwood cells, some N labile compounds exist; cf. Doucet et al. 2011). Stand successional phase might affect the N cycle, and tree size and ontogeny effects should also be considered since N is more abundant in the most recently formed rings of the sapwood. For instance, Van der Sleen et al. (2015) explicitly considered changes in tree size and age to adequately interpret series of tree-ring δ15N values in tropical forests. In their work, Borghetti et al. (2016) pioneered the potential use of wood-anatomical traits to unveil the effects of long-term N deposition on wood function, tree growth and forest productivity. Here we argue that while such studies give us an important starting point, they would gain support by addressing the existing caveats (tree size and ontogeny, plasticity, measuring and laboratory protocols) and by using other proxies of tree functioning such as δ15N in tree rings. Distilling information of environmental changes from wood is a demanding task but the rewards include gaining an improved knowledge of growth variability and the functioning of trees to better manage forests during the Anthropocene.

References Anderegg WRL, Schwalm C, Biondi F, et al. (2015) Pervasive drought legacies in forest ecosystems and their implications for carbon cycle models. Science 349:528–532. Anfodillo T, Carraro V, Carrer M, Fior C, Rossi S (2006) Convergent tapering of xylem conduits in different woody species. New Phytol 169:279–290.

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nutrition-designed experiments miss out on long-term synergistic interactions between these elements. A second point is related to tree size (mainly height) and ontogeny, which are the main determinants of the universal long-term changes in conduit lumen area as a plant ages and grows (West et al. 1999, Anfodillo et al. 2006, Olson et al. 2014). To properly understand changes in xylem anatomical attributes under rising levels of N and C availability, the increasing trend of conduit size during ontogeny must be clearly taken into account as indicated by Carrer et al. (2015). Thirdly, we still do not fully understand the level of environmental information imprinted in xylem anatomical traits. In this regard, many studies provided contrasting results: a much lower plasticity of wood traits with respect to leaf plasticity was observed in throughfall manipulation experiments that excluded precipitation and induced drought on Mediterranean tree species (Limousin et al. 2010). In contrast, with manipulative experiments based on seedlings or poplar saplings, other authors observed wider xylem vessels in response to increased N availability (Yazaki et al. 2005, Plavcová and Hacke 2012). In addition, a recent study in a tropical forest also found an increase in vessel diameter and a decrease in the frequency of small vessels with higher N and phosphorus availability, while vessel patterning tended to be more clustered (Spannl et al. 2016). The authors interpreted these changes as mechanisms to reduce cavitation risk in response to drought and provide sufficient water to the increased leaf area induced by N fertilization. Fourthly, we need manipulative experiments considering several different scenarios such as warming, drying, elevated ca and N deposition rates to thoroughly ascertain how functional anatomical traits contribute to tree acclimation. These experiments should be connected with mechanistic models linking increased N availability, growth rates and changes in wood anatomy. Lastly, N deposition rates are estimated through chemistry-transport models with critical uncertainty related to the emission inventories, particularly in some forest types (e.g. tropical forests, temperate forests from the southern hemisphere), which are currently under-represented in most analyses. For instance, the Borghetti et al. (2016) meta-analysis mostly included studies from Eurasia that are dominated by boreal, temperate and Mediterranean forest types. Long-term anatomy records would be very valuable for sites with oligotrophic soils such as the tropical dry forests where N-fertilized trees grow more and become more resistant to embolism (Bucci et al. 2006). To summarize, we need to discern if the effects of longterm N fertilization maximize C gain (increasing aboveground leaf biomass), enhance growth and alter hydraulic architecture at the cost of having trees with lighter wood (Goldstein et al. 2013).

Bridging wood functioning and nitrogen deposition

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