Jan Muhr

What's the flux? Unraveling how CO2 fluxes from trees reflect underlying physiological processes

Forum Commentary What’s the flux? Unraveling how CO 2 fluxes from trees reflect underlying physiological processes Tree stems and branches emit carbon dioxide (CO 2 ) at rates that per unit area can rival emissions from leaves or the soil surface and summed over a forest stand can comprise 14–30% of the total CO 2 efflux (Chambers et al., 2004; Ryan et al., 2009). Stem CO 2 fluxes have predictable patterns of variation with growth rate, stand age, and elevation (Chambers et al., 2004; Ryan et al., 2009; Robertson et al., 2010). Over the past decade observations of diel covariation of CO 2 efflux with sapflux rates measured in tree stems have led to the conclusion that internal transport of CO 2 within the stem strongly influences the measured CO 2 efflux at the surface (Teskey et al., 2008). In this issue of New Phytologist, Bloemen et al. (pp. 555–565) report on a tracer experiment that demonstrates not only upward transport of 13 CO 2 added to the transpiration stream, and emission of this label along the stem, but also fixation of a significant fraction of the added CO 2 in canopy branches, petioles and, to a minor extent, leaves. The study of Bloemen et al. adds to the growing literature that demonstrates the utility of isotope labeling studies to understand allocation and carbon (C) cycling in trees (Powers & Marshall, 2011; Epron et al., 2012). ‘Dynamic approaches for measuring continuous diurnal CO 2 fluxes and transport in the transpiration stream need to be more widely applied.’ Processes influencing stem CO 2 efflux A number of factors can influence the efflux of CO 2 measured by a flux chamber covering a segment of tree stem (Fig. 1). The cambium is the site of formation of new tissue, that is, of growth, while maintenance respiration produces CO 2 in all living tissues. The C being respired may derive from recent photosynthetic products transported in the phloem (e.g. Powers & Marshall, 2011) and from storage reserves. The pathways for respiration may vary with time or tree species: recently 18 O/ 16 O measurements in oxygen (O 2 ) provided the first evidence for the alternative oxidase pathway contributing to respiration in some tree stems (Angert et al., 2012a). CO 2 may also be locally fixed by photosynthetic tissues found under the bark before it is lost to the atmosphere. O 2013 The Authors New Phytologist O 2013 New Phytologist Trust Low rates of diffusion, especially across the cambium, can cause high CO 2 concentrations in stems, and internal O 2 concentrations can drop to very low levels (Spicer & Holbrook, 2005; Teskey et al., 2008). CO 2 is highly soluble, and will dissolve in (or exsolve from) stem water, depending on local saturation conditions, which in turn are controlled by factors such as temperature and pH. Uptake of CO 2 directly from the soil atmosphere, once thought potentially important, has largely been shown to be minor (see summary in Bloemen et al.). Hence the source of CO 2 emitted to the atmosphere from the bark surface can reflect a combination of local growth and maintenance respiration, other local processes producing CO 2 (including potentially decomposition in heartwood) or CO 2 from respiration in other tissues (e.g. roots) that has been transported into the volume beneath a chamber in solution. However, there can also be net export in the xylem water stream, as indicated by the fate of the tracer added by Bloemen et al. The measured chamber flux at any given time is thus the complex result of transport in, transport out and respiration minus photosynthesis in local tissues. Use of a dark chamber will exclude local photosynthesis. Observations of a relationship between sapflux and CO 2 efflux provide a clue as to whether CO 2 is net imported or exported from the volume of stem under a chamber attached to the stem surface (see Fig. 1, modified from Teskey et al., 2008). Other evidence for net CO 2 transport away from the region of efflux measurement comes from lower-than-expected efflux rates compared with what is expected given the construction costs of wood (Ryan et al., 2009), and potentially from higher efflux rates in canopy branches (Teskey et al., 2008). Changes in local temperature and/or pH can change respiration rates and also cause changes in CO 2 solubility (Kunert & Mercado Ca´rdenas, 2012). Stem anatomy, including bark thickness and tree hydraulics, likely influences the importance of the mechanisms and can help explain observations such as changes in CO 2 efflux with stand age or tree size, or differences between similar trees growing in different environments (Ryan et al., 2009). Bloemen et al. report results from labeling Populus deltoides, the eastern cottonwood tree, which has very high transpiration rates and generally is found in riparian zones. As noted by Ubierna et al. (2009) most studies that have reported relationships between sapflux and CO 2 efflux have been made in tree species with high sapflux rates and small conducting area. By contrast, the large conifer trees investigated by Ubierna et al. (2009), with lower overall sapflux, did not demon- strate such relationships, and even crown removal did not change the rates of CO 2 efflux from stems they studied. What do these results mean for interpretation of other ecosystem CO 2 efflux measurements? A major conclusion of Bloemen et al. is that the transport of the tracer from the tree base to the canopy indicates that root respiration New Phytologist (2013) 197: 353–355 353 www.newphytologist.com

How fresh is maple syrup? Sugar maple trees mobilize carbon stored several years previously during early springtime sap‐ascent

While trees store substantial amounts of nonstructural carbon (NSC) for later use, storage regulation and mobilization of stored NSC in long-lived organisms like trees are still not well understood. At two different sites with sugar maple (Acer saccharum), we investigated ascending sap (sugar concentration, δ(13) C, Δ(14) C) as the mobilized component of stored stem NSC during early springtime. Using the bomb-spike radiocarbon approach we were able to estimate the average time elapsed since the mobilized carbon (C) was originally fixed from the atmosphere and to infer the turnover time of stem storage. Sites differed in concentration dynamics and overall δ(13) C, indicating different growing conditions. The absence of temporal trends for δ(13) C and Δ(14) C indicated sugar mobilization from a well-mixed pool with average Δ(14) C consistent with a mean turnover time (TT) of three to five years for this pool, with only minor differences between the sites. Sugar maple trees hence appear well buffered against single or even several years of negative plant C balance from environmental stress such as drought or repeated defoliation by insects. Manipulative investigations (e.g. starvation via girdling) combined with Δ(14) C measurements of this mobilized storage pool will provide further new insights into tree storage regulation and functioning.

Carbon dioxide emitted from live stems of tropical trees is several years old

Storage carbon (C) pools are often assumed to contribute to respiration and growth when assimilation is insufficient to meet the current C demand. However, little is known of the age of stored C and the degree to which it supports respiration in general. We used bomb radiocarbon ((14)C) measurements to determine the mean age of carbon in CO2 emitted from and within stems of three tropical tree species in Peru. Carbon pools fixed >1 year previously contributed to stem CO2 efflux in all trees investigated, in both dry and wet seasons. The average age, i.e., the time elapsed since original fixation of CO2 from the atmosphere by the plant to its loss from the stem, ranged from 0 to 6 years. The average age of CO2 sampled 5-cm deep within the stems ranged from 2 to 6 years for two of the three species, while CO2 in the stem of the third tree species was fixed from 14 to >20 years previously. Given the consistency of (14)C values observed for individuals within each species, it is unlikely that decomposition is the source of the older CO2. Our results are in accordance with other studies that have demonstrated the contribution of storage reserves to the construction of stem wood and root respiration in temperate and boreal forests. We postulate the high (14)C values observed in stem CO2 efflux and stem-internal CO2 result from respiration of storage C pools within the tree. The observed age differences between emitted and stem-internal CO2 indicate an age gradient for sources of CO2 within the tree: CO2 produced in the outer region of the stem is younger, originating from more recent assimilates, whereas the CO2 found deeper within the stem is older, fueled by several-year-old C pools. The CO2 emitted at the stem-atmosphere interface represents a mixture of young and old CO2. These observations were independent of season, even during a time of severe regional drought. Therefore, we postulate that the use of storage C for respiration occurs on a regular basis challenging the assumption that storage pools serve as substrates for respiration only during times of limited assimilation.

Comparison of CO2 and O2 fluxes demonstrate retention of respired CO2 in tree stems from a range of tree species

The ratio of CO2 efflux to O2 influx (ARQ, apparent respiratory quotient) in tree stems is expected to 22 be 1.0 for carbohydrates, the main substrate supporting stem respiration. In previous studies of stem fluxes, ARQ 23 values below 1.0 were observed and hypothesized to indicate retention of respired carbon within the stem. Here, 24 we demonstrate that stem ARQ <1.0 values are common across 85 tropical, temperate, and Mediterranean forest 25 trees from 9 different species. Mean ARQ values per species per site ranged from 0.39 to 0.78, with an overall 26 mean of 0.59. Assuming that O2 uptake provides a measure of in situ stem respiration (due to the low solubility 27 of O2), the overall mean indicates that on average 41% of CO2 respired in stems is not emitted from the local stem 28 surface. The instantaneous ARQ did not vary with sap flow. ARQ values of incubated stem cores were similar to 29 those measured in stem chambers on intact trees. We therefore conclude that dissolution of CO2 in the xylem sap 30 and transport away from the site of respiration cannot explain the low ARQ values. We suggest to examine 31 refixation of respired CO2 in biosynthesis reactions as possible mechanism for low ARQ values. 32

Living on borrowed time – Amazonian trees use decade‐old storage carbon to survive for months after complete stem girdling

Summary Nonstructural carbon (NSC) reserves act as buffers to sustain tree activity during periods when carbon (C) assimilation does not meet C demand, but little is known about their age and accessibility; we designed a controlled girdling experiment in the Amazon to study tree survival on NSC reserves. We used bomb‐radiocarbon (14C) to monitor the time elapsed between C fixation and release (‘age’ of substrates). We simultaneously monitored how the mobilization of reserve C affected δ13 CO 2. Six ungirdled control trees relied almost exclusively on recent assimilates throughout the 17 months of measurement. The Δ14C of CO 2 emitted from the six girdled stems increased significantly over time after girdling, indicating substantial remobilization of storage NSC fixed up to 13–14 yr previously. This remobilization was not accompanied by a consistent change in observed δ13 CO 2. These trees have access to storage pools integrating C accumulated over more than a decade. Remobilization follows a very clear reverse chronological mobilization with younger reserve pools being mobilized first. The lack of a shift in the δ13 CO 2 might indicate a constant contribution of starch hydrolysis to the soluble sugar pool even outside pronounced stress periods (regular mixing).