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Lauriks F, Salomón RL, De Roo L, SteppeK. Leaf and tree responses of young European aspen trees to elevated atmospheric CO2 concentration vary over the season.
Abstract
Elevated atmospheric CO2 concentration (eCO2) commonly stimulates net leaf assimilation, decreases stomatal conductance and has no clear effect on leaf respiration. However, effects of eCO2 on whole-tree functioning and its seasonal dynamics remain far more uncertain. To evaluate temporal and spatial variability in eCO2 effects, one-year-old European aspen trees were grown in two treatment chambers under ambient (aCO2, 400 ppm) and elevated (eCO2, 700 ppm) CO2 concentrations during an early (spring 2019) and late (autumn 2018) season experiment. Leaf (stomatal conductance, net carbon assimilation and leaf respiration) and whole-tree (stem growth, transpiration and stem CO2 efflux) responses to eCO2 were measured. Under eCO2, carbon assimilation was stimulated during both the early (1.63-fold) and late (1.26-fold) season. Stimulation of carbon assimilation changed over time with largest increases observed in spring when stem volumetric growth was highest, followed by late season down-regulation, when the increase in stem volumetric growth ceased. The neutral eCO2 effect on stomatal conductance and leaf respiration measured at leaf scale paralleled the unresponsive canopy conductance (derived from sap flow measurements) and stem CO2
efflux measured at tree scale. Our results highlight that the seasonal variability in carbon demand for tree growth substantially affects the magnitude of the response to eCO2 at both leaf and whole-tree scale.
Introduction
Atmospheric CO2 concentration ([CO2]) has been rising rapidly since the industrial revolution (NOAA 2020), causing an overall increase in global mean air temperature and more irregular patterns in the hydrological cycle, hence challenging forests to grow and survive in increasingly harsh environments (Menezes-Silva et al. 2019). Forests are however expected to partially mitigate climate change effects (IPCC 2018) as ~30 % of the anthropogenically emitted CO2 is taken up through plant photosynthesis (Pugh et al. 2019). To better predict ongoing climate change, it is therefore essential to understand forests’ ability to sequester carbon (C) and survive under future climate conditions (Cernusak et al. 2019, Anderegg et al.
2020).
Elevated atmospheric [CO2] (eCO2) commonly stimulates net carbon assimilation (An) and decreases stomatal conductance (gs) at the leaf scale (Ainsworth and Rogers 2007, Ainsworth and Long 2020). More uncertainty exists on the response of leaf respiration (RL) under eCO2
conditions (Dusenge et al. 2019), precluding closure of leaf C budgets. Studies on RL have been contradictory, with reports of a positive (e.g. Wang et al. 2001), negative (da Silva et al.
2017) or neutral (e.g. Hamilton et al. 2001, Aspinwall et al. 2017) response to eCO2. The effect
of eCO2 on leaf scale processes (An, gs and RL) has been the main focus of eCO2 research over the past three decades. Nevertheless, whole-tree responses to eCO2 determine ecosystem C and water fluxes to a greater extent, and have been comparatively overlooked (Figure 1.3, Becklin et al. 2017). Predictions of whole-tree behaviour under eCO2 based on leaf scale observations have resulted in large discrepancies (Chapter 2, Table 2.2). For instance, eCO2-induced stimulation of An does not consistently translate into greater biomass production, especially in mature forests, suggesting C availability is not necessarily the most limiting factor for tree growth (Körner 2003, 2015, Palacio et al. 2014). Along the same line, regulation of the respiratory metabolism at the whole-tree scale under eCO2 remains quite uncertain (Smith 2017, Dusenge et al. 2019) despite its crucial role to determine tree and ecosystem net primary production (Valentini et al. 2000, De Lucia et al. 2007, Collalti and Prentice 2019). For instance, increase in gross primary production in a dry Eucalyptus woodland free air CO2 enrichment (FACE) experiment did not increase net primary production due to parallel stimulation of ecosystem respiratory fluxes (Jiang et al. 2020). Similarly, four years of eCO2 exposure in a 100-year-old mixed forest did not result in an increased stem growth (Asshoff et al. 2006) despite stimulation of An at the leaf scale (Zotz et al. 2005). The same idea applies to water relations. Reductions in gs under eCO2 do not necessarily result in water use limitations at the whole-tree scale due to large dependence of whole-tree water use on canopy leaf area (LA), where potential LA stimulation under eCO2 can offset the decrease in leaf scale water loss (Tor-ngern et al. 2015, Fatichi et al. 2016). As a result, whole-tree water use might decrease (Wullschleger and Norby 2001), increase (Tricker et al. 2009) or remain unaffected (Ward et al. 2013, Tor-ngern et al. 2015) under eCO2 regardless of the stomatal behaviour at the leaf scale.
Besides the spatial variability, leaf and tree responses to eCO2 (hereafter ‘eCO2 effects’) are also dynamic over time. The magnitude and direction of eCO2 effects vary with leaf age and over a single growing season (Chapter 2). Seasonal canopy and root development, stem biomass production, reproduction, leaf senescence and growth cessation shift the balance between C sources and sinks year-round, affecting tree responsiveness to eCO2 and feedback mechanisms. As a result, in well-watered Eucalyptus globulus trees, eCO2-induced stimulation of An was stronger in summer (+46 %) than in winter (+14 %) (Quentin et al. 2015), and in Tilia americana trees An stimulation was variable with leaf age and across the season, with strongest eCO2 effect during spring and in young leaves (Li et al. 2019b). Time-dependent stimulation of An under eCO2 also translated into a dynamic stimulation of stem and whole-tree growth, with stronger eCO2 effects during spring and summer compared to autumn and winter (e.g. Yazaki et al. 2004, Bigras and Bertrand 2006). Similarly, the magnitude of gs
reduction under eCO2 has also been observed to vary over the season with strongest gs
reductions during early and mid-summer, after which the eCO2 effect dwindled towards the onset of autumn (Tissue et al. 1997, Wullschleger et al. 2002a). Nonetheless, gs reduction under eCO2 is not always observed (Xu et al. 2016) and the effect of eCO2 on gs can substantially differ depending on the exposure time to eCO2 (Medlyn et al. 2001), the functional plant type (evergreen vs. deciduous plant species; Medlyn et al. 2001, Dusenge et al. 2019) and the environmental conditions, in particular water availability (Goodfellow et al.
1997), making stomatal behaviour under eCO2 more difficult to predict.
Further exploration of eCO2 effects at a fine temporal resolution (on a sub-daily basis) reveals complex interactions among plant water and C relations (Steppe et al. 2015). At leaf scale, highly resolved measurements under eCO2 have shown sub-daily variability in leaf expansion rate of Populus (Walter et al. 2005) and species-specific (for P. tremula, P. tremuloides and Sambucus racemosa) temporal shifts of the daily maximum gs during the day (Batke et al.
2020), all affecting sub-daily water and C budgets. Nonetheless, sub-daily dynamics in whole-tree processes under eCO2 remain relatively unexplored (Wullschleger and Norby 2001, Tricker et al. 2009, Dawes et al. 2014). In 36-year-old Larix decidua trees, daily stem shrinkage measured with point dendrometers was reduced under eCO2, presumably as a result of altered stem water flow and storage under eCO2 (Dawes et al. 2014). In Liquidambar styraciflua trees, a general sap flow (SF, as proxy of transpiration) reduction was observed under eCO2 throughout diurnal hours (Wullschleger and Norby 2001). Contrastingly, in a P. x euramericana stand and on days with high atmospheric water demand, increased canopy LA under eCO2 resulted in stimulation of SF, but effects were larger before noon than during the afternoon (Tricker et al. 2009). Although largely unexploited to date, sub-daily dynamics in stem diameter variations, whole-tree water use as a proxy for transpiration and stem CO2
efflux under current and future CO2 regimes might provide novel insights in eCO2-induced alterations in tree C and water relations.
The objective of this study was to assess variability in eCO2 effects on leaf and whole-tree physiology during two seasonal stages: start and end of the growing season. To this end, one-year-old European aspen (Populus tremula L.) trees were subjected to ambient (aCO2) and elevated (eCO2) atmospheric [CO2] in two subsequent growing seasons. Point leaf measurements (An, gs and RL) and continuous stem measurements (stem diameter variations, SF and stem CO2 efflux) were used to evaluate the temporal and spatial variability in leaf and tree responses to eCO2. We hypothesized that (i) eCO2 will stimulate leaf An and overall respiration as a consequence of increased tree growth, and will reduce leaf gs and hence whole-tree water use, (ii) leaf scale processes will be more susceptible to eCO2 than whole-tree processes, and (iii) stronger eCO2 effects will be observed at the beginning of the growing season, followed by a down-regulation towards the onset of autumn.