Nitrogen supply and other controls of carbon uptake of understory vegetation in a boreal Picea abies forest

Agricultural and Forest Meteorology 276–277 (2019) 107620

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Nitrogen supply and other controls of carbon uptake of understory vegetation in a boreal Picea abies forest

T

Sari Palmrotha,b, , Lisbet H. Bachc, Marie Lindhc, Pasi Kolarid, Annika Nordine, Kristin Palmqvistc ⁎

a

Division of Environmental Science & Policy, Nicholas School of the Environment, Duke University, Durham, NC, 27708-0328, USA Department of Forest Ecology & Management, Swedish University of Agricultural Sciences (SLU), SE-901 83, Umeå, Sweden c Department of Ecology & Environmental Sciences, Umeå University, SE-901 87, Umeå, Sweden d Institute of Atmospheric and Earth System Research, Helsinki University, FI-00014, Finland e Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences (SLU), SE-901 87, Umeå, Sweden b

ARTICLE INFO

ABSTRACT

Keywords: Coniferous forest Dwarf shrub Field layer Hydraulic traits Photosynthetic capacity Canopy photosynthesis model

In boreal forests, carbon (C) uptake by understory may be too large to be ignored and too variable in space to be assumed a constant fraction of the ecosystem gross primary production. To improve estimates of understory production in these ecosystems, we need to better account for its main controls. In this study, we estimated C uptake of field-layer vegetation, dominated by Vaccinium myrtillus, V. vitis-idaea, and Deschampsia flexuosa, in a boreal Picea abies stand in northern Sweden. Nitrogen (N) availability in the stand has been manipulated through annual N additions since 1996 at the rates of 0, 12.5, and 50 kg N ha−1 yr−1. To assess the relative importance of N supply, and interannual fluctuations in leaf biomass and weather, in controlling field-layer photosynthetic production, we calculated C uptake over eight growing seasons using a canopy photosynthesis model. Without N additions, tree leaf area index (L) was already high (8.5) and field-layer C uptake was small, 27 g C m−2 (or ∼3% of stand C uptake). An increase in tree L with N additions further reduced light availability for the understory, yet the concurrent increase in the relative abundance of the more physiologically active D. flexuosa sustained the contribution of the field-layer to stand photosynthetic production. Based on a literature survey, in which site quality or stand age generated a wide range in L, understory contribution to ecosystem C uptake increases linearly with the fraction of available light reaching the forest floor across high latitude forests. Understory contributes only ∼5% to ecosystem C uptake where trees intercept ∼80% of incoming light, increasing to 100% after clearcut tree harvest. While the availability of solar energy, both spatially and temporally, is the primary driver of understory production, our analyses suggest that the predicted increases in drought severity and frequency at high latitudes may affect understory communities more than trees. Future empirical and modeling studies should focus on functional and ecological responses to drought of not only trees but also understory species, which contribute to biodiversity and convert their photosynthates to important non-timber products.

1. Introduction The boreal forest is estimated to contribute ∼20% to the total carbon (C) sink of the world’s forests (Pan et al., 2011). Most studies quantifying ecosystem C inputs, i.e., gross primary production or C uptake, focus on trees. Compared to trees, the amount of biomass of, and the absolute C uptake by the understory plants are small under closed tree canopies, where overstory intercepts most of the available solar energy (Kolari et al., 2006; Misson et al., 2007). However, in open stands, typical of nutrient poor sites common in boreal forests, understory vegetation may contribute > 50% of ecosystem C uptake (Goulden and Crill, 1997; Ikawa et al., 2015). Part of this production,

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e.g., in the form of wild berry yields, is also of economic importance, particularly in Fennoscandia (Kardell, 1980; Miina et al., 2009). Moreover, because of the higher turnover rate of the forest understory biomass, its role in ecosystem carbon and nutrient cycling is likely disproportionate to its biomass fraction (Nilsson and Wardle, 2005). Taken together, the role of C uptake of understory plant communities is too central to be ignored in carbon balance assessments through measurements or ecosystem models and too variable from stand to stand to be assumed a constant faction of the ecosystem flux across landscapes. Ecosystem-atmosphere gas exchange can be estimated from chamber and eddy-covariance measurements and, where the understory and overstory fluxes are measured separately, the relative

Corresponding author at: Nicholas School of the Environment, Box 90328, Duke University, Durham, NC, 27708-0328, USA. E-mail address: [email protected] (S. Palmroth).

https://doi.org/10.1016/j.agrformet.2019.107620 Received 11 September 2018; Received in revised form 10 May 2019; Accepted 11 June 2019 Available online 19 June 2019 0168-1923/ © 2019 Elsevier B.V. All rights reserved.

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contribution of each canopy layer to the net ecosystem C exchange can be discerned (Misson et al., 2007; Kolari et al., 2006; Kulmala et al., 2011a,b, 2019; Ikawa et al., 2015). However, net ecosystem C exchange is the balance between C taken up in photosynthesis and that released in ecosystem respiration, and each process responds differently to changes in the environment. Thus, disentangling the responses of, e.g., canopy photosynthesis to fluctuations in resource availability, requires additional assumptions and modeling steps (Lasslop et al., 2010) and is particularly challenging when it comes to understory fluxes. Also, the flux tower sites represent a small fraction of the variation contained in the vast boreal forest (Kasurinen et al., 2014), where climate, soils, and plant communities vary greatly (Bergeron et al., 2007; Ikawa et al., 2015; Boonstra et al., 2016), and the measured fluxes are thus difficult to scale up to the landscape, region, and beyond. This requires using alternative approaches that enable studying the variability in, and interactions among growing conditions, e.g., nutrient supply and weather, within any given region or vegetation community type. Combining better understanding of the main drivers of understory photosynthetic production within and among ecosystems with models, may offer the best approach to assess the contribution of the understory to ecosystem energy and material cycling. Carbon uptake can be calculated using canopy gas exchange, or flux models that are based on climate, canopy structure, and leaf physiology, i.e. on physical and physiological processes (Fig. 1a). These models vary in complexity and application. The more complex models include detailed descriptions of the canopy structure and can reproduce gas exchange rates at sub-daily resolution, by species and canopy layers, and cover a variety of responses to environmental changes (Mäkelä et al., 2006; Launiainen et al., 2015, 2016; Minunno et al., 2016). When used in conjunction with resource/climate gradients or controlled experiments, such as fertilization, drought or elevated CO2, the structural and physiological responses to a treatment/perturbation can be accounted for in the model inputs (e.g., leaf area) and in the parameterization of the physiological processes (e.g., maximum carboxylation rate and plant hydraulic conductance). Such detailed investigations can inform large-scale ecosystem models and help identify conditions when (if ever) simplifications can be justified in direct upscaling of measurements across ecosystems. For instance, it makes intuitive sense that C uptake of understory is inversely related to overstory light interception. Yet, it is not clear which stand component, e.g., tree canopy leaf area index affecting energy

availability to the understory, or understory biomass integrating the effects of site quality and energy availability for photosynthesis, can be used as proxies for understory C uptake. This study focuses on the Fennoscandian boreal coniferous forest, where ecosystem productivity is limited by short growing seasons and, in most cases, nitrogen (N) availability, and where forest management (e.g., fertilization, harvesting, planting) and global warming may either alleviate or exacerbate these limitations (Gauthier et al., 2015; Högberg et al., 2017). These ecosystems are dominated by conifers, Pinus sylvestris (Scots pine) and Picea abies (Norway spruce). Undisturbed, pure P. sylvestris stands are more common on dry, low-fertility soils and P. abies is found in closed stands on more nutrient-rich sites (Esseen et al., 1997). While ericaceous dwarf shrubs predominate the field layer in the understory, species composition ranges from sparse field layer and almost pure lichen-moss ground cover to herb-rich field-layer communities along gradient of site quality. The relative abundance of the two most common dwarf shrubs, Vaccinium myrtillus (bilberry) and V. vitisidaea (lingonberry), peaks on the low-to-mid fertility sites. These species show a fairly broad and similar optimum, and the stand-to-stand variability of their relative and absolute biomass is likely driven by light and water availability rather than fertility (Mäkipää, 1999). A study on these two species growing in the Alps demonstrated that, while they appear similar in their hydraulic traits, V. vitis-idaea recovers faster from drought than V. myrtillus and can thus colonize drier sites (Ganthaler and Mayr, 2015). Except for excessively drained sites and years with unusually low rainfall, ecosystem C uptake and productivity in the Fennoscandian boreal forest are generally not considered water limited (Duursma et al., 2009; Kulmala et al., 2011b; Lim et al., 2015, 2017), yet water supply may vary among species or species groups depending on, e.g., rooting depth. Similar to natural site quality gradients, where increasing N supply alters the distribution of intercepted energy between over- and understory, fertilization experiments suggest that N additions result in increased tree foliage biomass and volume growth (Axelsson and Axelsson, 1986; Sigurdsson et al., 2013; Lim et al., 2015; From et al., 2016) and changes in understory species composition (Mäkipää, 1999; Strengbom et al., 2002; Gundale et al., 2014). The effects on species composition can be direct (growth of some species respond more than others), or indirect, where the abundance dynamics is affected by fluctuations in pathogen and herbivore populations (Nordin et al., 2009). That is, biotic stressors may respond positively to increased N

Fig. 1. (A) Schematic presentation of the canopy and the main components of the canopy photosynthesis model used in this study. Environmental drivers include air temperature (Tair), photosynthetic photon flux density (PPDF), atmospheric water vapor pressure deficit (D), precipitation (P), and volumetric soil moisture content (θ) and nitrogen (N) addition as the experimental manipulation. Plant physiological inputs include whole plant hydraulic conductance (kL) and leaf physiological parameters i.e. maximum carboxylation capacity (Vcmax) and maximum electron transport rate (Jmax). (B) Interannual variability in the leaf biomass of Vaccinium myrtillus, V. vitis-idaea, and Deschampsia flexuosa at Svartberget Experimental Forest. N addition treatments [0 (Control), 12.5 (N1) and 50 (N2) kg N ha−1 year−1] commenced in 1996. Leaf biomass estimates calculated in this study are based on pin-point intersect measurements, conducted annually 1995–2009 and every three years thereafter (Nordin et al., 2009, A. Nordin, unpublished data). Error bars represent standard error (n = 6); estimates with no error bars are based on linear interpolation. 2

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supply causing reduction-recovery cycles in their host plant abundance. Due to changes in species composition, N additions may have little impact on the long-term (steady state) average total field-layer biomass but likely reduce that of ground-layer mosses (Gundale et al., 2014). Fertilization has been shown not to affect allocation of growth between above- and belowground parts or leaf physiological activity (light saturated photosynthetic rate and stomatal conductance) of V. myrtillus and V. vitis-idaea despite an increase in leaf N concentration (Palmroth et al., 2014). Here, we aimed at quantifying the responses of C uptake of fieldlayer plants to N additions in a boreal coniferous stand. We assessed the relative importance of key physiological traits, canopy structural changes, and environmental variables in controlling annual photosynthetic production. The study was conducted in a P. abies dominated stand in the Svartberget Experimental Forest in northern Sweden, where soil nitrogen N availability has been amended through N additions of 0, 12.5, and 50 kg N ha−1 yr−1 since 1996 (Nordin et al., 2005). The three most abundant field-layer species are: V. myrtillys, V. vitis-idaea, and Deschampsia flexuosa (wavy hair-grass), of which D. flexuosa exhibits the highest photosynthetic capacity (Kulmala et al., 2009). We hypothesized (H1) that the interannual variability in the C uptake of field-layer species in this mesic forest is driven mostly by energy availability and temperature, while water availability plays a limited role (Kulmala et al., 2011b; Lim et al., 2015). With increasing N availability and main canopy light interception, we expected the C uptake of the two dwarf shrubs to decrease (Palmroth et al., 2014). At the same time, the relative abundance of D. flexuosa has increased with N supply (Fig. 1b; Nordin et al., 2009), and we hypothesized (H2) that these two opposing trends result in similar annual field-layer C uptake across the N addition treatments. We estimated C uptake of the field-layer by species using a canopy photosynthesis model, Stand Photosynthesis Program (SPP; Mäkelä et al., 2006; Duursma et al., 2008, 2009) and use it as a diagnostic tool to disentangle and quantify the main contributors to variation in C uptake. We parameterized the radiative transfer and the coupled leaf photosynthesis-stomatal conductance modules in SPP (Farquhar et al., 1980; Leuning, 1995) for each N addition treatment with data collected in this study and used local canopy structural and environmental data to calculate hourly C uptake over eight growing seasons.

based on photosynthetically active radiation intercepted by the foliage (Oker-Blom et al., 1989) and a biochemical photosynthesis model coupled with an empirical stomatal conductance (gs) model, where gs varies photosynthetic rate and atmospheric vapor pressure deficit (‘Farquhar-Leuning’ model, Farquhar et al., 1980; Baldocchi, 1994; Leuning, 1995). The effect of soil water limitation on gas exchange via stomatal regulation is described with the ‘embolism avoidance’ soilplant water flow model by Duursma et al. (2008). The model describes the behavior of isohydric plants with constant leaf-specific plant hydraulic conductance and daily minimum leaf water potential, but variable conductance from soil to root. 2.2.1. SPP inputs and parametrization 2.2.1.1. Environmental data. We estimated species-specific C uptake of plants growing in each of the three N addition treatments (C, N1, and N2) from April 5 to November 1 over a period of eight years (2006–2013) at a constant atmospheric CO2 concentration of 390 ppm. Hourly weather data (incoming photosynthetic photon flux density, air temperature, precipitation, and relative humidity; Fig. 2ab; Table S1) were obtained from a nearby weather station. Volumetric soil moisture content was measured in 2009–2013, at 6-to-12-cm depth in the mineral soil, in a nearby, similar stand (with respect to species composition and age) growing on the same soil type as our study stand, at the Krycklan Catchment Study (Laudon et al., 2013). The full list of climatic drivers in the SPP model as well as a set of plant physiological and structural input parameters for a boreal Pinus sylvestris stand (referred to as ‘default parameterization’ from hereon)

2. Methods 2.1. Experimental setup The experiment was performed at Svartberget Experimental Forest (64°14′N, 19°46′E) in Vindeln, northern Sweden. Details of the site and the N addition experiments are given by Nordin et al. (2005). Briefly, the Svartberget stand is dominated by 120-year-old Picea abies (L.) Karst. trees growing on a gently sloping moraine (glacial till). The field layer includes Vaccinium myrtillus L., V. vitis-idaea L. and Deschampsia flexuosa L., and the bottom layer is composed of Hylocomium splendens (Hedw.) Br. Eur., and Pleurozium schreberi (Brid.) Mit. Annual mean temperature (1981–2010) in the study area is 1.8 °C and precipitation 614 mm (Laudon et al., 2013). The background atmospheric N deposition rate in this area is 1–2 kg N ha−1 year−1 (Phil-Karlsson et al., 2009). Nitrogen addition commenced in 1996 and consists of six replicate square plots (1000 m2) of each treatment [0 (C), 12.5 (N1) and 50 (N2) kg N ha−1 year−1] in a randomized block design. 2.2. Estimating stand C uptake

Fig. 2. Daily variation of selected model inputs from 2011: (A) Photosynthetic photon flux density (PPFD), air temperature (Tair), and atmospheric water vapor deficit (D); (B) precipitation (P), and volumetric soil moisture (θ); (C) leaf area index (L) relative to maximum L for Picea abies, Vaccinium myrtillus, V. vitisidaea, and Deschampsia flexuosa, and state of acclimation of photosynthesis (S for V. myrtillus, in relative units) describing the lagged effect of past temperatures on photosynthetic performance (Mäkelä et al., 2004).

We used the Stand Photosynthesis Program (SPP) to estimate C uptake of both field-layer and overstory vegetation. SPP was developed and tested for boreal and temperate coniferous stands (Mäkelä et al., 2006; Duursma et al., 2008, 2009). In SPP, the canopy is divided into volume elements and photosynthetic rate in each element is calculated 3

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can be found at wiki.helsinki.fi/display/∼[email protected]/SPP. The P. sylvestris is growing on glacial till at the Helsinki University SMEAR II (Station for Measuring Forest Ecosystem-Atmosphere Relations) research station in Hyytiälä, Finland (61° 51′ N, 24° 17′ E). In our SPP runs, we used site-specific values for a subset of parameters (as described below), keeping the rest at their default values.

expressed as a linear function of S (Fig. 2c; Kolari et al., 2007) such that their values ranged between 10 and 100% of their maximum values. The values of τ for the field-layer species were taken from Kulmala et al. (2011b). To evaluate the ability of SPP to reproduce leaf C uptake rates of V. myrtillys and V. vitis-idaea, we measured leaf gas exchange and leaf water potentials (ΨL, including predawn water potentials, protocol described below) over the course of one day, July 6, 2013. We sampled individuals at random locations (both open and shaded) from C and N2 plots. We set the Li-Cor 6400XT leaf chamber conditions to follow ambient conditions and, after each gas exchange measurement, we estimated the chamber leaf area and bagged the shoot for ΨL measurements with a pressure chamber (PMS Instrument Company, Albany, OR). We calculated hourly leaf gas exchange using SPP, and averaged the estimates over the two treatments and species.

2.2.1.2. Stand structure. In SPP, a coniferous tree layer is described as randomly distributed crowns (ellipsoids in this study) filled with spherically-oriented shoots (the unit of annual growth). The necessary model inputs include stand density, tree height, crown width and length, leaf area index (L), and the ratio of shoot silhouette to total leaf area that quantifies light interception efficiency (similar to extinction coefficient; Stenberg et al., 1995). Leaves of all understory (shrubs or herbaceous) species are randomly distributed within the understory canopy volume. Thus, plant height, L, leaf orientation, and light extinction coefficient (mean leaf projection; Stenberg, 2006) by species are needed as inputs. The details of the data collection of the plant structural characteristics for this study are described in Supplementary Materials. Briefly, for each treatment, we estimated maximum L of the field-layer species annually, while the maximum L of P. abies was measured once and assumed to be constant (at a steady state) across years. To account for intra-annual dynamics in L, the fraction of overwintering leaf area was set based on leaf longevity (or the number of age classes present) to 0.85 of the maximum L for P. abies and 0.5 for V. vitis-idaea, from which L was growing daily from bud break until a threshold temperature sum was reached, whereas leaf senescence was driven by day length (Fig. 2c; Mäkelä et al., 2006). The L dynamics of V. myrtillus and D. flexuosa were derived following Jonasson and Chapin (1985), amended with local snow depth records and other phenological observations (M. OttosonLöfvenius, pers. comm.).

2.2.1.4. Stomatal and whole-plant hydraulic conductance. We measured stomatal conductance (gs) responses to varying atmospheric water vapor deficit (D) of current-year leaves of V. myrtillus and one-yearold leaves of V. vitis-idaea under semi-controlled conditions. In May 17–28 of 2013, around the time of leaf flush, we extracted patches (0.6 × 0.4 x 0.15 m) of the understory vegetation and the organic layers (down to the bottom of root systems at the top of the mineral soil) from C and N2 plots, and placed them in 12 and 15 trays, respectively. At the end of May, the trays were transferred to Umeå campus of the Swedish University of Agricultural Sciences, kept in partial shade outdoors and watered as needed until the measurements took place in July 10 August 3. The day prior to measurements, we took a subset of trays into a growth chamber (with day/night set at 18/6 h, day/night air temperature at 20/16 °C, daytime RH at ∼80% and PPFD at ∼400 μmol m−2 s-1). The following day, we measured gas exchange on one individual per tray and species. The leaf chamber conditions were set to 20 °C and PPFD to 400 μmol m−2 s−1, with a range of D from 0.6 to 2.2 kPa (5–6 levels) obtained by scrubbing water vapor from the incoming air. After each change in D, we waited for at least 30 min before recording the gas exchange rates. We measured five gs-to-D curves per species and treatment and estimated the area of each sampled leaf. The curves were analyzed following Oren et al. (1999): gs = gsref− m*ln(D), where gsref (mol m−2 s−1) is gs at D = 1 kPa and m is the rate of change in gs per unit of change in D (dgs/dln(D)). The sensitivity of gs to D thus obtained was compared with the predictions of the Leuning model in SPP. In August 15–28, 2013, we estimated whole-plant, leaf-specific hydraulic conductance (kL, mmol s−1 m−2 MPa−1) of individuals growing in C and N2 plots based on: kL = 1/ AL × E/( L S) (Franks, 2004), where AL is the leaf area (m2) of the shoot, E is H2O exchange rate (mmol s−1), and ΨL and ΨS are given in MPa. Note that, in SPP, the soil-to-root hydraulic conductance is treated separately from the rootto-leaf conductance (Duursma et al., 2008) and, thus, our estimates of kL are not directly comparable to these two components. Also, ΨS is calculated in SPP based on soil volumetric water content and soil texture (Clapp and Hornberger, 1978). For our on-site kL estimation, we used predawn leaf water potential (ΨLpd) as a proxy for ΨS. The night before the measurements, we covered a 4 × 4-m patch of ground vegetation in each treatment with black plastic sheet to prevent transpiration. The following morning, five individuals per species were collected from the middle of the covered area and bagged for shoot ΨLpd measurements. Midday E was measured on five individuals (three leaves per individual) of each species and treatment at PPFD of 400 μmol m-2 s−1 and otherwise close-to-ambient chamber conditions (∼20 °C and ∼1 kPa). The shoots were then bagged and their ΨL and AL were measured/estimated. To extend the range of conditions under which ΨL and ΨLpd were determined, we repeated these measurements in July 2014, on the same two species and following the same protocol, in a nearby P. sylvestris stand. This stand, growing on a sandy soil was subject of an experiment including the same annual N addition rate

2.2.1.3. Photosynthetic parameters. The Farquhar model parameters (Farquhar et al., 1980), maximum carboxylation capacity (Vcmax25) and maximum electron transport rate (Jmax25), were estimated from A/ ci -curves, where A is CO2 exchange rate and ci leaf-internal CO2 concentration, based on measurements taken between June 20 and July 3, 2012. We sampled healthy, dominant individuals of V. myrtillus, V. vitis-idaea, and D. flexuosa from one 1000-m2 plot in each treatment (C, N1, and N2) and from patches where all species experienced similar microenvironments. For the dwarf shrubs, an individual refers to a single ramet, an aboveground shoot arising from a belowground rhizome. Gas exchange measurements in this study were carried out with 1–4 open gas exchange measurement systems (Li-Cor 6400XT with 640002B red/blue light source and 20 x 30 mm chamber; Li-Cor Biosciences, Lincoln, NE, USA). Five to seven mature individuals/leaves (1-year-old leaves for V. vitis-idaea) were sampled in from each treatment. Leaf CO2 and H2O exchange rates were measured at 20 °C, 50–70% relative humidity, and saturating PPFD (500–800 μmol m−2 s-1), and at 9–12 CO2 concentrations, from 50 to 2000 μmol mol-1. Following the completion of a response curve, the leaf (or leaves) in the chamber were collected, scanned and their area estimated using ImageJ (rsbweb.nih.gov/ij/). We did not measure gas exchange on P. abies in this study but used parameter values reported by Medlyn et al. (2005; Vcmax25 of 21, Jmax25 of 51 μmol CO2 m−2 s-1, expressed here per unit all-sided leaf area). In SPP, the fast temperature responses of key photosynthetic parameters are adopted from Collatz et al. (1991), while the slow acclimation of photosynthetic capacity to prevailing temperature is described with the ‘state of acclimation’ model, or the S model (Mäkelä et al., 2004; Kolari et al., 2007, 2014). The state of acclimation reflects the temperature photosynthetic machinery is acclimated to. It depends on temperature, and a time constant (lag, τ) that controls the window of time of temperature history influencing the current photosynthetic capacity. In this study, the photosynthetic parameter values were 4

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(N2, 50 kg N ha−1 yr−1; Lim et al., 2015) as in our P. abies stand. Note that the conditions in the leaf chamber, where fans increase air circulation (and boundary layer conductance), can be different from what the leaves experience outside, depending on leaf characteristic dimension (Jarvis and McNaughton, 1986). While the absolute measures of kL obtained in this way are likely overestimates, particularly at high E and/or small ΨS- ΨL, they are useful for studying relative differences among species (with similar leaves) and across treatments or sites.

3. Results and discussion 3.1. Leaf physiology and plant hydraulic conductance across N addition treatments Of the three field-layer species, D. flexuosa showed the highest maximum carboxylation capacity (Vcmax25) and maximum electron transport rate (Jmax25), followed by V. vitis-idaea and V. myrtillus (Table 1). The photosynthetic parameters did not change with N additions (P ≥ 0.672, ANOVA) likely reflecting increased overstory L with N supply and reduced light availability for the understory (Palmroth et al., 2014). Stomatal conductance (gs) of well-watered V. myrtillus and V. vitisidaea individuals declined with increasing water vapor deficit (D), such that the higher the reference gs at D = 1 kPa (gsref; Fig. 3a) the faster was the decline of gs with increasing D. The mean ratio between dgs/dLn (D) and gsref (dashed line) indicates that, under these conditions, these plants appeared to be less sensitive to changes in D than would be expected for isohydric plants with strict stomatal control of leaf water potential to avoid excessive embolism (black line; Oren et al., 1999). A conclusive assessment of an/isohydry, however, would require additional gas exchange and leaf water potential measurements across a wider range of soil water availability (Martınez-Vilalta et al., 2014). The high N addition treatment (N2) seemed to have reduced gsref (treatment means indicated with dotted symbols) of V. vitis-idaea (P = 0.027, t-test) but not of V. myrtillus (P = 0.273). While a decrease in gsref indicates decreased sensitivity of gs to variations in D (Fig. 3a inset), based on our SPP simulations, high-D-induced stomatal closure occurs rarely in the mostly cool and humid summers, making these differences inconsequential in terms of plant C uptake (Fig. 2a, Table S1). Similar fertilization-induced reductions in gsref have been observed in temperate and boreal tree species, often accompanied with reductions in hydraulic conductance throughout the hydraulic pathway (Domec et al., 2009, 2016; Ewers et al., 2000; Ward et al., 2008, 2013). In this study, we found no clear between-species or -treatments differences in leaf-specific hydraulic conductance (kL) at any given leaf water potential (Ψ L) for the two dwarf shrubs (Fig. 3b). Because the dataset collected in the understory of the P. abies stand did not cover an overlapping range in midday ΨL to allow proper testing for differences among species and treatment relationships, we augmented it by collecting data in a nearby P. sylvestris stand (open symbols in Fig. 3b). In this second dataset, neither the treatments nor the species clearly separated (P ≥ 0.072, ANCOVA). Hence, our findings appear to be in line

2.3. Statistical analyses In all analyses based on ecophysiological measurements we used individual (leaf or shoot) as the sampling unit. For measured variables, and when appropriate, we tested for differences among species and treatments using t-test, ANOVA, or ANCOVA. Non-linear functional relationships were linearized prior to testing. All statistical analyses were carried out with either Sigmaplot 12 or Systat 13 (Systat Software Inc, San Jose, CA, USA). For all modeled C uptake estimates, if standard error was given, it was calculated based on temporal (interannual) variation only. Evaluation of the model-structure, and parameterization-related uncertainties in SPP were evaluated in detail earlier (Duursma et al., 2008, 2009) and is out of scope of this study. Table 1 Maximum carboxylation capacity (Vcmax25) and electron transport rate (Jmax25) at a leaf temperature of 25 °C expressed per unit projected (scanned) leaf area for three understory species: Vaccinium myrtillus, V. vitis-idaea and D. flexuosa. Nitrogen addition treatments at Svartberget are 0 (Control), 12.5 (N1), and 50 kg ha−1 year−1 (N2). Standard error is given in parenthesis and n is the sample size. Species V. myrtillus V. vitis-idaeaa D. flexuosa

a

Control N1 N2 Control N1 N2 Control N1 N2

Vcmax25

Jmax25

n

26.4 28.9 24.9 41.1 44.2 38.8 83.6 86.7 98.6

46.0 (2.2) 55.9 (9.7) 51.1 (3.0) 84.0 (6.9) 88.8 (11) 77.5 (5.3) 128 (6.4) 134 (4.1) 130 (3.8)

5 4 5 5 3 5 5 3 6

(3.3) (5.4) (2.6) (4.4) (6.9) (4.9) (9.4) (6.9) (8.8)

For 1-year-old leaves.

Fig. 3. (A) Slope of stomatal conductance (gs) response to varying atmospheric vapor pressure deficit (dgs/dLn(D)) as a function of gsref (gs at D = 1 kPa) for Vaccinium myrtillus and V. vitis-idaea. Dotted symbols indicate averages by species and N addition treatment [0 (Control) and 50 (N2) kg N ha−1 year−1]. Shown are the theoretical ratio between dgs/dLn(D) and gsref (black line; Oren et al., 1999), the statistical fit to all data (grey line), and the Leuning-model (dashed line) prediction: gs = g0 + a1 A/[(cs Г)(1 + D/D0)], were the fixed parameters are: g0 = 0.002 mol m−2 s−1, a1 = 5, Cs = 390 μmol mol−1, Г = 31 μmol mol−1, D0 = 1 kPa, and where gs was calculated for D ranging from 0.5 to 2.3 at photosynthetic rates (A) ranging from 2 to 12 μmol m−2 s-1. (A inset) The Leuning-model gs-D relationship for V. vitis-idaea with a1 = 7 (C, solid line) and a1 = 5 (N2, dashed line). (B) Leaf-area-specific hydraulic conductance (kL) as a function of leaf water potential (ΨL). Small symbols represent data from a nearby Pinus sylvestris stand. 5

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with those by Ganthaler and Mayr (2015), who demonstrated that these two Vaccinium species are similar with respect to most hydraulic traits. For a snapshot validation of SPP, we compared measured and simulated leaf CO2 exchange rates over a typical summer day in 2013 (Fig. 4a). The measured rates (points in Fig. 4b) represent the two Vaccinium species, sampled form both open and shaded locations. The two SPP-based diurnal courses (lines), in turn, depict average rates across treatments and species. The dashed line, enveloping the measured data, represents open conditions, and the solid line, falling within the lower half of the measured range, represents the average conditions for field-layer species under the main canopy. As a model validation, this comparison is rather limited; however, it indicates a reasonable agreement between the measured and modeled leaf-level C uptake rates. Further, we complemented the comparisons with a rough grounding of the modeled annual C uptake estimates. Using aboveground net primary production (NPPA) estimates for V. myrtillus, representative of conditions in canopy openings (Palmroth et al., 2014), and corresponding C uptake (GPP) estimated here, resulted in ratios between the two ranging (across treatments) from 0.22 - 0.36, or NPP/ GPP from 0.44 to 0.49 (assuming NPP/ ANPPA = 1.75; Gower et al., 2001), which are within reasonable limits for boreal ecosystems (Goulden et al., 2011; Tang et al., 2014). Leaf water potentials, measured during the same day and averaged across treatments and by hour, showed a typical diurnal course of first declining and then stabilizing such that, during the day, ΨL of V. vitisidaea, stayed consistently more negative that of V. myrtillus (Fig. 4c). Moreover, the measured predawn water potentials (Fig. 4c), were more negative than the bulk soil water potential (ΨS) calculated in SPP. A similar difference between measured predawn and modeled soil water potentials was observed during the kL measurement campaign (not shown). This may indicate a mismatch between the conditions at the depth of 6-to-12-cm in the mineral soil, reflected in the modeled ΨS, and that of the rooting zone of the field-layer plants, mostly in the humus and the uppermost mineral soil layer (Makkonen and Helmisaari, 2001). 3.2. Effects of intra- and interannual variation in weather on C uptake We studied the effects of variation in the amount of incoming solar energy and air temperature on modeled C uptake through simulations with other main drivers held constant, i.e. with fixed peak leaf area of field-layer and assuming that soil moisture availability was not limiting C uptake. Averaged over the eight-year study period for each species, 28–40% of the carbon uptake occurred in July (Fig. 5a). For the evergreen V. vitis-idaea, approximately 25% of the total uptake occurred outside the three warmest summer months, indicating that it is likely to be better buffered against droughts or other stress events occurring during the warmest months compared to the deciduous V. myrtillus. While the monthly C uptake followed air temperature (not shown), the climatic driver explaining most of the interannual variation in photosynthetic production was the cumulative photosynthetically active radiation (PPFD) at the top of the main canopy and, particularly, direct PPFD (Fig. 5b, black symbols). This reflects the fact that the mean growing-season temperature was better correlated with direct PPFD than total PPFD (r = 0.75 and 0.57, respectively). We then assessed the potential drought effects on the field-layer C uptake over the years, for which volumetric soil moisture (θ) data were available (2009–2013, Table S1). During that period, the measured θ never dropped below 0.15 m3 m−3 and the corresponding estimates of Ψ S were never low enough to trigger stomatal closure in SPP sufficient to reduce plant C uptake. However, when the model was calibrated, by adjusting the parameters of the soil water retention curve in SPP to match ΨS estimates with measured predawn ΨL, the C uptake estimates dropped (Fig. 5b, grey symbols). They were, on average, 9% and up to 23% lower compared to rates calculated with no soil moisture limitation (black symbols). These findings suggest that, in contrast to our first

Fig. 4. (A) Diurnal course of photosynthetic photon flux density (PPFD) and atmospheric water vapor deficit (D) on July 6, 2013. (B) Measured CO2 exchange rates on Vaccinium myrtillus (black symbols) and V. vitis-idaea (grey symbols) leaves over the course of the day. Modeled (SPP) CO2 exchange rates averaged across treatments (solid line) and rates simulated for open conditions (dashed line). Symbols represent different N addition treatments: [0 (Control, circles) and 50 (N2, triangles) kg N ha−1 year−1]. (C) Measured predawn and daytime leaf water potentials (ΨL) of the two shrubs averaged across treatments, and modeled (SPP) soil water potential (ΨS) for the site. Error bars indicate standard error across individual shoot samples (n = 5–8).

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Fig. 5. (A) Monthly C uptake relative to growing season C uptake for Vaccinium myrtillus, V. vitis-idaea and Deschampsia flexuosa. Error bars represent variation across years, standard error (n = 8). (B) April-to-October C uptake (averaged across species) relative to the mean C uptake across years as a function of cumulative direct photosynthetic photon flux density (PPFD). Relative fluxes estimated assuming no soil water limitation on C uptake (black symbols, years 2006–2013; r2 = 0.82) and when soil drought is accounted for (grey symbols, years 2009–2013).

hypothesis (H1), soil water availability may indeed be a significant driver of field-layer photosynthesis. The more severe drought spells, as was experienced in 2018 in the region, and anticipated in the future (Allen et al., 2010) may reduce C uptake more regularly by amounts similar to the typical fluctuation in year-to-year solar energy input and temperature. These conclusions on drought responses reflect the SPP model structure as well as some key assumptions related to the environmental data we used as input. First, in SPP, variation in ΨS is the most important control of the hydraulic limitation of stomatal opening (Duursma et al., 2008). To better capture the actual ΨS, we calibrated the modeled ΨL to match the measured predawn ΨL. However, plant water status may not equilibrate with that of the soil if transpiration continues through short summer nights (Sellin, 1999). We minimized night-time transpiration by covering patches of understory the night before all pre-dawn ΨL measurements. However, because a single rhizome can extend several meters (Flower-Ellis, 1971), even the areal shoots in the middle of the covered patches may have been connected to transpiring ones. This would lead to predawn ΨL more negative than the actual ΨS, and to overestimation of the soil drought effect on C uptake. Second, given similar parameterization, the model-based responses of C uptake to soil drought were the same across species and treatments. Yet, it is quite plausible that the species varied in their ability to recover from the loss of hydraulic conductivity following drought spells (Ganthaler and Mayr, 2015) potentially causing carryover effects to subsequent drought-rewetting cycles. As embolism and recovery (refilling) is not considered in SPP (i.e. plants strictly regulate

water potential), our analyses would have missed such differences had they occurred. 3.3. Effects of N additions on C uptake The mean overstory leaf area index (L ± coefficient of variation, CV %) in the C, N1 and N2 plots were estimated at 8.5 ± 4, 8.3 ± 21, and 11.0 ± 6, respectively. The responses of field-layer C uptake to N supply, when variations in tree L, leaf physiology and biomass, and weather conditions were included, mostly reflected those of leaf biomass, within and across species (Figs. 1 and 6). Of the three species, the contribution of V. vitis-idaea to field-layer C uptake was the smallest and further decreased with increasing rate of N additions. While the higher N supply reduced carbon uptake of V. myrtillus, the estimates of absolute and relative (to the total field-layer) C uptake of D. flexuosa increased with both N addition rates. The eight-year cumulative C uptake was somewhat lower in the control and high N addition plots, with mean rates ( ± CV% across years) of 27 ± 12 and 30 ± 15 g C yr−1, than under the low N additions with mean rate of 35 ± 24 g C yr−1. Had the only response to the high N application been a change in the main canopy L, the 23% higher L compared to the control conditions would have resulted in a 16% decline of the field-layer photosynthesis (triangle in Fig. 7). However, in support to our second hypothesis (H2), the field-layer C uptake did not decline under high N additions, due to an almost threefold increase in the mean annual biomass of D. flexuosa (Fig. 1), the species with the highest physiological activity of the three. Fig. 6. (A) April-to-October C uptake of Vaccinium myrtillus (black symbols), Deschampsia flexuosa (dark grey), and V. vitisidaea (light grey) for fertilized plots as a function C uptake of the control plots. Line represents 1:1 relation. (B) Cumulative C uptake over the period of 2006–2013 across N addition treatments. Color scheme is the same as in (A).

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driven seasonality in photosynthetic capacity and L, typical for boreal species, is captured in SPP (Mäkelä et al., 2004, 2006; Kolari et al., 2007, 2014), interactions among abiotic factors (weather conditions) and leaf traits (leaf mass per area or leaf longevity) were not accounted for due to lack of data at adequate temporal resolution. Finally, our C uptake estimates represent three field-layer species only. For a rough estimate of the moss photosynthetic production, we combined biomass estimates for feather moss at the same site from Gundale et al. (2014), and an estimate of C uptake (per unit moss biomass) from a mature P. sylvestris stand in Finland (Kulmala et al., 2011b), and calculated growing-season fluxes of 30, 23, and 14 g C m−1 for the control, N1 and N2 plots, respectively. These moss C uptake estimates reflect large reductions in feather moss biomass with increasing rate of N addition reported by Gundale et al. (2014). The estimated contribution of moss layer to understory C uptake hence varied from 29% (N2) to 53% (C), the total understory C uptake being the highest in the non-fertilized plots. 3.4. Variation in understory C uptake across boreal stands Fig. 7. C uptake of field layer and trees, relative to C uptake estimated for control plots (tree leaf area index, L = 8.5), as a function of the fraction of photosynthetically active radiation intercepted by trees (fPART). fPART changes with grouping of trees in clumps of 3–20 (circles with hourglass) and with increasing L, where the filled triangles represent L of 11 (as in plots with high N additions).

To explore ways to generalize the findings on the contributions of understory photosynthesis to ecosystems C uptake across boreal stands, we combined our data with other published estimates (see Supplementary Materials). The published production estimates were either based on direct flux measurements (included all understory vegetation) or modeling (by species) and some of the following comparisons are thus based on field-layer fluxes (Fig. 8abc) while others represent total understory C uptake (Fig. 8d; including ours, where the moss C uptake is estimated as described above). The Fennoscandian stands in the combined dataset formed two groups based on soils: stands growing on sites of somewhat lower productivity (glacio-fluvial deposits) and those growing on better sites (glacial till). At high light availability below the main canopy (i.e. low fraction of photosynthetically active radiation intercepted by trees, fPART), the two groups separate in their photosynthetic efficiency of the field-layer C uptake, and in absolute production, while the groups merge under more shaded conditions (Fig. 8ab). The two groups collapse into one when photosynthetic production was plotted against the amount of field-layer leaf biomass, a variable that integrates the effects of two important drivers of C uptake, light availability and site quality (Fig. 8c). One may then ask whether the C uptake rate of a forest with dense overstory of trees is higher than a more open forest with both overstory and understory? For these Fennoscandian sites, the estimates of ecosystem C uptake (Fig. 8b) for closed tree canopies were higher than stands without an overstory of trees (clearcut administered 5–6 years prior to the assessments; Kulmala et al., 2009, 2011b). Note, however, that the ecosystem C uptake of the open (no overstory trees) sites is underestimated as the photosynthetic production of the tree seedlings was not accounted for. Moreover, additional data are needed to assess the shape of the trajectory between the two endpoints, i.e. whether there are any among-species interactions in their resource use and productivity. In relative terms, across stands in the American and Eurasian boreal zone (Fig. 8d), the understory C uptake relative to that of the ecosystem decreases with increasing main canopy light interception. Based on this analysis, understory contributes ∼5% of ecosystem C uptake where trees intercept ∼80% of the incoming light, ∼40% at fPART of 50%, naturally approaching 100% after clearcut tree harvest. Taken together, higher N supply results in lower amount of solar energy available for the understory, yet N-fertilization-induced changes in the field-layer species composition may partially compensate for the effect of reduced light on its C uptake. However, increased tree L with N supply, and, thus, interception of precipitation and transpiration of trees (Tor-ngern et al., 2017, 2018), may lead to faster reduction of water availability to understory species between precipitation events. Indeed, in contrast to trees that have access to water stored deeper in

A key driver of the understory productivity is the amount of solar energy transferred through the main canopy, which depends on both the amount of leaf area and its spatial distribution. In SPP, foliage in a coniferous canopy is grouped into shoots, randomly distributed inside crowns of individual trees, which are, in turn, randomly located in the stand. Of these structural determinants of canopy light interception, the assumption of random distribution of trees in space is likely the least valid in our study stand (Stenberg et al., 2014). To simulate the effect of non-randomness in tree locations on the field-layer photosynthesis, we placed the trees into groups of 3–20, but kept tree dimensions and canopy L fixed (circles with hourglass in Fig. 7). Increasing the size of the groups of trees (and openings at a given L) resulted in moderate reductions of the main canopy light interception and C uptake (grey symbols to the left of the vertical line) and larger relative increases in C uptake by the understory (black symbols). This analysis suggests that, all else being equal, our estimates of the fieldlayer C uptake (∼30 g C m−2 yr-1 for the control treatment) may represent a conservative, lower end of the range of potential flux estimates. In contrast, based on an estimate calculated with main canopy removed, the field-layer C uptake may reach ∼70 g C m−2yr-1 in the middle of a large gap. Furthermore, these flux estimates are based on calculations where the leaf angles of the field-layer species are either horizontal (Vaccinium) or spherically distributed (D. flexuosa) representing our best assessments of the distributions. Had the leaf angle distributions of the shrubs also been described as spherical, the fieldlayer C uptake estimates would have dropped by 28–45% depending on the treatment. While these can be taken as rough bounds around the estimates, further structural measurements would be needed to quantify the net effect of the two potential errors (of opposing signs) on fieldlayer C uptake. Ecosystem-level, indirect effects of N additions were not fully incorporated in our C uptake estimates. Common herbivores and pathogens are known to have large interactive effects on V. myrtillus productivity (Strengbom et al., 2002; Nordin et al., 2005, 2009). Our calculations account for the year-to-year variation in leaf biomass, which, at least partially, reflects the severity and year-to-year dynamics of defoliation. However, the within-season reduction in active leaf area (or leaf physiological activity) and photosynthetic production caused by biotic stressors were not considered. Further, while the temperature8

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Fig. 8. (A) Field-layer C uptake per unit leaf biomass (Lmass), (B) field-layer (closed symbols) and ecosystem (field layer + mosses + trees; open symbols) C uptake as a function of the fraction of photosynthetically active radiation intercepted by trees (fPART), and (C) field-layer C uptake as a function of Lmass. (D) Decrease in the fraction of understory C uptake of ecosystem C uptake with increasing fPART. Data from this study (closed circles, squares, and triangles, as in Fig. 1), Kulmala et al. (2009, 2011a,b; stars), and from other studies (open circles; Black et al., 1996; Goulden and Crill, 1997; Hollinger et al., 1998; Constantin et al., 1999; Bergeron et al., 2007; Xue et al., 2011; Ikawa et al., 2015; Kulmala et al., 2019). In (D), understory C uptake estimates include field-layer and moss. Regression line: y = -1.19x + 0.995, R² = 0.91, P < 0.001.

Appendix A. Supplementary data

the mineral soil, shallow-rooted understory species may experience more frequent and severe drought-related reduction in understory C uptake if growing season precipitation decreases in the future (Allen et al., 2010). Studies focusing on understory species are needed to better predict the long-term effects of repeated severe droughts on understory species composition and C fluxes. Finally, where N availability, together with other attributes of site quality, or stand age, generate a wide range in L, understory contribution to photosynthetic production decreases with the amount of light reaching the forest floor similarly across the Boreal Forest. Thus, at a coarse scale, the first approximation of the relative contribution of understory photosynthesis to ecosystem production can be estimated based on the fraction of incoming light intercepted by the tree canopy.

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Author contributions SP, AN, KP conceived the study; SP, LB, MR performed research; SP, LB, MR, PK analyzed data; SP, LB, PK, AN, KP wrote the paper. Acknowledgements The authors wish to thank Ann Sehlstedt, Otilia Johansson, and Mikael Ottosson Löfvenius for their assistance with field and lab work, and with processing of environmental data. This project was part of a joint research program founded by FORMAS (grant 2010-67) between the Swedish University of Agricultural Sciences and Umeå University on ‘Sustainable Management of Carbon and Nitrogen in Future Forests’. S.P. also acknowledges the support the US Department of Energy (DOE) through the Office of Biological and Environmental Research (BER) Terrestrial Carbon Processes (TCP) program (DE-SC0006967). 9

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