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Article

Long-Term Warming and Nitrogen Addition Regulate Responses of Dark Respiration and Net Photosynthesis in Boreal Bog Plants to Short-Term Increases in CO2 and Temperature

by
Thuong Ba Le
1,2,3,4,
Jianghua Wu
1,2,*,
Yu Gong
1,2,5 and
Mai-Van Dinh
6
1
Environment and Sustainability, School of Science and the Environment, Memorial University of Newfoundland, Corner Brook, NL A2H 5G4, Canada
2
Graduate Program in Environmental Science, Memorial University of Newfoundland, St. John’s, NL A1B 3X7, Canada
3
Department of Silviculture, Vietnam National University of Forestry, Hanoi 13417, Vietnam
4
Centre For Boreal Research, Northern Alberta Institute of Technology, Edmonton, AB T6H 3S5, Canada
5
Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan 430084, China
6
School of Science, Vietnam National University, Hanoi 144, Vietnam
*
Author to whom correspondence should be addressed.
Atmosphere 2022, 13(10), 1644; https://doi.org/10.3390/atmos13101644
Submission received: 11 August 2022 / Revised: 29 September 2022 / Accepted: 4 October 2022 / Published: 9 October 2022
(This article belongs to the Section Biosphere/Hydrosphere/Land–Atmosphere Interactions)
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Abstract

:
Boreal bog plants adapted to cold and low available nutrient conditions might be strongly affected by global changes, including elevated CO2 (eCO2), warming (W), and increasing nitrogen (N) availability. Here, we examined responses of dark respiration (Rd) and net photosynthesis (Anet) in four dominant bog plants to five levels of short-term increases in both CO2 and temperature (CTI); and the effects of long-term (6 years) W and N addition on these responses. Results indicated that CTI increased Rd; meanwhile, the increase of these environmental variables decreased Anet in all these boreal bog plants. Long-term nitrogen addition simulated the increases of Rd and decreases of Anet in Trichophorum cespitosum. Long-term warming mitigated the increases of Rd in Andromeda glaucophylla and Gaylussacia bigeloviana, and the decrease of Anet in Gaylussacia bigeloviana. These findings highlight the importance of long-term warming and nitrogen addition in regulating responses of boreal bog plants to short-term CTI, suggesting the necessity to investigate the long-term effects of these environmental changes when projecting responses of boreal bog vegetation to global changes.

1. Introduction

Photosynthesis and respiration are key physiological processes that regulate the carbon balance of individual plants, ecosystems, and the global carbon cycle [1,2]. Both are strongly affected by climate change resulting from increasing levels of atmospheric CO2 and other greenhouse gas concentrations [1,3,4,5]. Therefore, the responses of physiological processes to climate change should be viewed in direct relation to elevated CO2 (eCO2) conditions [6,7,8,9,10]. Plant photosynthesis and respiration are also greatly influenced by the soil environment, particularly its composite nutrients [11,12,13], which are affected by high nitrogen (N) deposition [14,15,16]. Hence, the effects of the concomitant increase in atmospheric CO2 and air temperature (CTI) on plant photosynthesis and respiration should be examined in evolving soil environments [3,8,11,17].
Boreal bogs are crucial ecosystems in the global carbon cycle [9,18], storing approximately 500 Gt carbon in belowground layers [19]. Boreal bog plants have been long-term adapted to the permanent water saturation, cold, acidic, and low available nutrient conditions [20,21,22]; therefore, the plants may be susceptible to predicted environmental changes, including climate change [23] and increased levels of available N concentration [24]. The increases in temperatures may benefit vascular plants [25,26] and depress Sphagnum [27,28,29,30]. Similarly, increases in N concentration might interrupt N competition from Sphagnum [31], leading to more abundance of boreal bog vascular plants [29,32,33,34,35]. Therefore, the concomitant warming (W) and N-enrichment conditions may significantly profit vascular plants and inhibit Sphagnum mosses in boreal bogs. In addition, the increases in atmospheric CO2 may enhance the photosynthesis of boreal bog plants as in other ecosystems [36]. However, the responses of boreal bog plants to the predicted environmental changes in photosynthesis and respiration have not been studied
In response to this knowledge gap, we designed a complete factorial experiment including W and N addition in 2014 at a typical boreal bog in Western Newfoundland, Canada. By utilizing portable gas exchange analyzers (Li-6400 XT), the experiment enabled us to investigate responses of net photosynthesis (Anet) and dark respiration (Rd) in four dominant species (i.e., one Sphagnum moss, two shrubs, and one graminoid species) to the short-term concomitant eCO2 and air temperature increases after the plants were exposed to the long-term (6 years) warming and enriched N conditions. We hypothesize that: (1) Short-term CTI will increase the Rd in these boreal bog plants, and the positive effects of the short-term CTI on Rd will be accelerated by long-term N addition, meanwhile, be reduced by W; (2) the short-term CTI will increase Anet in vascular plants (two shrubs and one graminoid), the positive effects of CTI on Anet will be stimulated by long-term W and N addition; (3) the short-term CTI will decrease Anet in Sphagnum, the responses of Anet in the moss will be reduced by the long-term exposure to W and be stimulated by long-term N addition.

2. Materials and Methods

2.1. Study Site

The study site is situated at an ombrotrophic blanket bog located in Robinsons, western Newfoundland, Canada (48°15′44″ N, 58°40′03″ W). The last 30-year annual air temperature and precipitation were approximately 5 °C and 1340 mm, respectively [37]. In the 2020 growing season (from 1 May to 30 September), the mean air temperature was 12.9 °C, and the total precipitation was 286.2 mm, respectively. The bog has a 3 m depth peat with a pH of 4.5 in groundwater [38]. The study site is a typical boreal bog in Newfoundland, where a bryophyte layer of Sphagnum mosses dominates vegetation. The vascular plant community consists of dwarf shrubs (Andromeda glaucophylla, Chamaedaphne calyculata, Gaylussacia bigeloviana, Vaccinium oxycoccus, Gaylussacia baccata, Rhododendron tomentosum, and Rhododendron groenlandicum), and graminoids (Rhynchospora alba, Trichophorum cespitosum).

2.2. Experimental Design

The experiment was conducted in 2014 and was described by Gong, et al. [37]. Specifically, four different treatments: Control (C), N fertilization (N), W, and a combination of N fertilization and W (NW), were randomly arranged in 4 plots at each block. Each plot covers an area of 4 m2 (2 m × 2 m) and is separated by 2 m buffer zones. To create 3 repetitions of the treatments, 3 blocks that include the four treatments were set up with 6m buffer zones between these blocks.
To simulate W, we used open-top chambers (OTCs) composed of six glass sheets (80 cm along the bottom edge, 62.5 cm along the top edge, and 40 cm in height) to cover an area of 1.66 m2. The W treatments increased the average daily air temperature at canopy level (20 cm aboveground) during growing seasons by 2.10 and 2.12 °C in 2019 and 2020, respectively. Therefore, we used this warming treatment to reflect a future climate scenario with a warming target of 1–2 °C.
To generate saturated conditions of available N in N and NW treatments, we applied two doses of 3.2 g N m−2 in early June and July each year from 2014 to 2018. In 2019 and 2020, four doses of 1.6 g N m−2 were applied monthly from June to September. The applications added 6.4 g N m−2 y−1 to the N and NW treatments. We wanted to generate a saturated available N leading to a N non-limited condition. The dose is ten times higher than annual N deposition in this study area [38], and comparable to the level of nitrogen addition in other studies on boreal peatlands [15,39,40,41,42,43]. Fertilizer was given in the soluble form (NH4NO3) dissolved in 2 L of the same site pool water. The C and W treatments were also watered with 2 L of water taken from the same pool at the same site without the N addition. The N addition did not change pH in N and WN plots.
To examine the responses of Anet and Rd to the CTI in dominant boreal bog plants, we set up five levels of CTI, including C400T0, C421T1.5, C538T2.3, C670T3.3, and C936T5.2. In detail, C400T0 indicates a present condition of CO2 (400 ppm) and temperature at the beginning of measurements in control plots (Toc), C421T1.5 (eCO2: 421 ppm, eT: Toc +1.5 °C), C538T2.3 (eCO2: 538 ppm, eT: Toc +2.3), C670T3.3 (eCO2: 670 ppm, eT: Toc +3.3), C936T5.2 (eCO2: 936 ppm, eT: Toc +5.2). These CTI levels indicate the present climate and 4 climate change scenarios, including representative concentration pathway 2.6 (RCP2.6), RCP4.5, RCP6.0, and RCP8.5 in the year 2100 in this study area [44,45]. Other conditions, such as photosynthetically active radiation (PAR) and relative humidity (RH), were constantly controlled during the leaf gas exchange measurements. Light saturation conditions (1500 µmol·m−2·s−1 in PAR) and 55–65% RH were stably controlled during Anet and Rd measurements in vascular plants. A lower PAR (500 µmol·m−2·s−1) and a higher RH (65–75%) were established during the Anet and Rd measurements in moss species. The conditions during measuring Anet and Rd in vascular species were generated by a Li-6400 XT (Li-COR Biosciences, Lincoln, NE, USA) with a red-blue light-emitting diode (LED) light source (6400-02B) and the standard 2 cm × 3 cm chamber. By contrast, a bryophyte chamber (6400-24) with a light source (6400-18A RGB) was used to create conditions during measuring the Anet and Rd of mosses.

2.3. Foliar Photosynthesis and Dark Respiration Measurements

We selected four dominant plant species because of their high coverage, including Sphagnum fuscum (S. fuscum), Trichophorum cespitosum (T. cespitosum), Andromeda glaucophylla (A. glaucophylla), and Gaylussacia bigeloviana (G. bigeloviana). In each plot, two individuals of A. glaucophylla and G. bigeloviana, one tussock of T. cespitosum, and 1 point of S. fuscum were labeled for 2-time gas exchange measurements when the leaves of the species were mature. These species have different leaf sizes, therefore, we clipped the different number of leaves during measuring Anet and Rd for these plants to ensure these leaves fit with the chamber and without overlapping between them. In detail, one leaf of G. bigeloviana, or 3–5 leaves of A. glaucophylla, or six leaves of T. cespitosum were selected for the Anet and Rd measurements in these plants by standard 2 cm × 3 cm chamber. With S. fuscum, six capitula (1cm from the top) of the species were cut from the labeled points, and these capitula were used for one-time measurement of Anet and Rd in the bryophyte chamber.
Anet was measured in the order of C400T0, C421T1.5, C538T2.3, C670T3.3, C936T5.2, and Rd measurement occurred at least 5 min after switching the light source off. Data was logged when reference CO2, chamber air temperature, and gas exchange levels were stabilized (CV < 1% over 20 s). After the measurements, the vegetation samples were collected and dried at 60 °C until the constant weight was used in computing Anet and Rd. These gas exchange measurements were conducted in two periods of the growing season, including the mid-growing season (from late July to early August) and the late-growing season (from late August to early September), when the plant leaves were mature.

2.4. Environmental Measurements

Air temperature (Tair) at the canopy level in each plot was measured at the beginning of Anet measurements. During the Anet and Rd measurement, a ProCheck sensor (Decagon Devices Inc., Pullman, WA, USA) was used to measure soil moisture (Msoil) and soil temperature (Tsoil) at 5 cm depth. Also, one MacroRhizon sampler (Rhizosphere Inc., Wageningen, The Netherlands) and a perforated PVC tube (sealed in the bottom permanently and capped at the top) were installed in each plot to collect soil pore water at 10 cm and 40 cm depths, respectively. In each Anet and Rd measurement sequence, the soil water samples were collected twice (the first collection two weeks before and the second one during the sequence). The water samples were filtered through 0.45-µm Cole-Parmer nylon membranes before analyzing NH4+ and NO3− concentration utilizing flow injection analysis methods (Lachat Instruments, Inc., Milwaukee, WI, USA).

2.5. Statistical Analysis

Data were processed and analyzed by R software ver. 3.6.3 [46]. The effects of CTI, W, N, season, species, and their interactions on Anet and Rd of 4 dominant boreal bog plants during the two periods of the growing season were analyzed utilizing mixed effect models, with experimental blocks as a random effect in nlme package [47]. After confirming the significant effects of season, species, and their interactions in the above models (Table S1), data split by the species and season. These splits were used to analyze the effects of CTI, N, W and their interaction on Anet and Rd of each species in the mid and late-growing season, separately, via utilizing mixed effect models, with experimental blocks as a random effect. The data were tested for normality, and Johnson transformation was used where necessary before analysis. Adjusted R2 of the models was computed by the rsq package [48]. To test the effects of CTI levels on Anet and Rd, a posthoc analysis was conducted by Tukey test in a multcomp package [49]. Mixed effect models were also used to examine the effects of N addition and W on the total cover of vegetation and environmental variables with experimental blocks as a random effect in the two periods of the growing season. All figures were created using ggplot2 [50] and ggpubr [51] packages.

3. Results

We found that species, seasons and their interactions significantly affected both Rd and Anet in boreal bog plants (Table S1). Therefore, we focus on analysis effects of CTI, W, N and their interactions on Rd and Anet by specises and seasons, and the detail results are shown in following sections.

3.1. The Response of Dark Respiration

The CTI significantly affected the Rd in four dominant boreal bog plant species (A. glaucophylla, G. bigeloviana, S. fuscum, and T. cespitosum) during both mid and late-growing seasons (p < 0.0001) (Table 1). The rise of CTI from C400T0 to C421T1.5 increased Rd in A. glaucophylla by 27% during the late-growing season (Figure 1h), while this change of CTI did not affect Rd in A. glaucophylla during the mid-growing seasons (Figure 1g) and Rd in other plants during both mid-and late-growing seasons (Figure 2g,h, Figure 3g,h and Figure 4g,h). Rd in the four boreal bog plants dramatically increased when the CTI increased from C400T0 to C538T2.3, C670T3.3, and C936T5.3 with an average of approximately 1.5 times, 3.2 times, and 7.6 times, respectively.
Moreover, Rd increases due to the CTI were regulated by N and W (Table 1). A significantly interactive effect (F1,38 = 4.1, p = 0.0071) between N and CTI on Rd was detected in T. cespitosum during the mid-growing season. In particular, N accelerated the increases of Rd due to C670T3.3 and C936T5.2 by 30% and 25%, respectively (Figure 4g). In contrast, W reduced the positive effects of CTI on Rd in A. glaucophylla in the mid-growing season (F4,38 = 7.9, p = 0.0076) and G. bigeloviana in the late growing season (F4,38 = 10.6, p = 0.0045). In detail, W dampened the increase of Rd in A. glaucophylla in C670T3.3 by 23% and C936T5.2 by 30% during the mid-growing season (Figure 1g). W also modified the effects of CTI on Rd in G. bigeloviana during the late growing season in the C670T3.3 and C936T5.2 conditions with 29% and 30% decreases, respectively (Figure 2h). However, W and N have no interaction effects on the response of Rd to CTI in all measured plants (Table 1).

3.2. The Response of Net Photosynthesis

Results show that Anet of 4 dominant boreal bog plants was significantly influenced by CTI during mid-and late-growing seasons (p < 0.0001) (Table 2). Anet of the plants had no change when CTI increased from C400T0 to C421T1.5 (Figure 1, Figure 2, Figure 3 and Figure 4). The increase of CTI to C538T2.3 only decreased the Anet of S. fuscum by 2.3-times during the late growing season (Figure 3j). C670T3.3 decreased Anet in all plants (Figure 2i, Figure 3i,j and Figure 4i,j), except A. glaucophylla during both periods of the growing season (Figure 1i,j) and G. bigeloviana during the late-growing season (Figure 2j). The lowest values of Anet were observed at C936T5.2 in all plants (Figure 1, Figure 2, Figure 3 and Figure 4). Of the four plants, S. fuscum showed the most significant Anet decreases due to CTI, with 3-times and 9-times lower at C936T5.2 than C400T0 during the mid and late-growing seasons, respectively (Figure 3i,j). By contrast, A. glaucophylla had the smallest decreases of Anet, with 34% and 39% decreases at the highest level of CTI during the mid and late-growing seasons, respectively (Figure 1i,j).
Moreover, we found that long-term N and W regulated the responses of Anet to CTI (Table 2). N accelerated the decreases in Anet of T. cespitosum by 34% and 95% during the mid-growing season when CTI increased to C670T3.3 and C936T5.2, respectively (Figure 4i). By contrast, W reduced the decrease of Anet in G. bigeloviana due to C936T5.2 by 93% during the late-growing season (Figure 2j). Furthermore, a combined effect of N and W on the responses of Anet to CTI was found in T. cespitosum during the late-growing season (F4,38 = 4.5, p < 0.01). W reduced the negative effect of N addition on Anet in T. cespitosum due to C936T5.2 during the late-growing season (Figure 4j).

3.3. Effects of W and N Addition Treatment on Environments

W significantly affected Tair, Msoil, and Tsoil during both the mid-growing season and late-growing seasons (p < 0.001), while the W did not influence NH4+ and NO3− in soil water samples (Table S2). Specifically, mean Tair was higher in the W treatment plots than in the control plots by approximately 3.2 °C during the mid-growing season and by 2.5 °C during the late-growing season (Table 3). Mean Tsoil was higher in the W treatment plots than in the control plots by approximately 3.6 °C during the mid-growing season and by 3.3 °C during the late-growing season (Table 3). Mean Msoil was 11% during the mid-growing season and 33% during the late-growing season at the W treatment plots, which were dramatically lower than in the control plots with 36% and 74% during the mid and late-growing seasons, respectively (Table 3).
N addition strongly influenced concentrations of NH4+ (p < 0.05) and Msoil (p < 0.001), while the treatment had no effects on NO3−, Tair, or Tsoil (p > 0.05) (Table S2). The mean concentration of NH4+ increased 3-times at 10 cm depth and 2-times at 40 cm depth during both mid-and late-growing seasons (Table 4). Msoil in the N plots was significantly lower than in the control plots, especially during the mid-growing season, with only 16% (Table 3).
We found the combined effects of W and N on Msoil during both mid and late-growing seasons (p < 0.001), as well as on Tsoil during the mid-growing season (p < 0.05) (Table S2). W enhanced the negative effects of N on soil moisture by 8% and 37% during the mid and late-growing seasons, respectively (Table 3). N reduced the increase of Tsoil due to W by 25% during the mid-growing season (Table 3).

4. Discussion

Boreal bogs have long been recognized as crucial ecosystems with a large carbon stock [19] due to unique features such as low temperature and low available nutrients [20,21,22]. However, there is increasing evidence that boreal bogs are subject to elevated CO2, warmer and N-enriched conditions due to climate changes [52,53], and/or rising N deposition [14,54]. These changes in CO2, temperature, and nutrients may significantly affect these bogs [16,23,24,55,56]. Here, we provide evidence that short-term CTI increased Rd and decreased Anet in boreal bog plants, which were regulated by long-term warmer, N-enriched treatments.

4.1. Responses of Dark Respiration

Previous studies have focused on the individual effects of temperature elevation (eT) or eCO2 on Rd, while the combined impact of these environmental changes on Rd is understudied [8]. Regarding responses of Rd to eCO2, previous studies have shown idiosyncratic results on the response of foliar Rd to eCO2, including increases [57,58,59]; no effects [60,61,62]; and, decreases [60,63,64]. Meanwhile, significant increases in Rd due to eT have been consistently observed in several previous experiments [1,62,65,66,67].
In this study, we did not examine the individual effects of eCO2 and eT on Rd; instead, we tested the effects of the concomitant increase in CO2 and temperature projected under future climate scenarios [44,45] in our study area. Results indicated that eCT significantly increases Rd in our dominant boreal bog plant species (Figure 1g,h, Figure 2g,h, Figure 3g,h, and Figure 4g,h, Table 1). The findings are in line with previous studies that suggest eT increases Rd [1,62,65,66,67]. These results indicate the possibility of temperature playing a dominant role in stimulating Rd under eCO2, high-temperature conditions [8,62,68].
We found that responses of Rd to CTI were modified by long-term N addition (Table 1). N addition accelerated the increases in Rd due to high levels of CTI in T. cespitosum by approximately 25-30% during the mid-growing season (Figure 4g). There is evidence to indicate the positive effects of leaf N concentration on Rd [69,70,71] and on the response of Rd to eCO2 [58,72]. The increases in mitochondrial density and size due to N addition [71] may accelerate Rd under high CTI conditions.
This study also revealed that the increase of Rd due to CTI was regulated by long-term W in two boreal bog shrubs, including A. glaucophylla during the mid-growing season and G. bigeloviana during the late-growing season (Table 1). Exposure to the 6-year W treatment reduced the positive effects of CTI on Rd by approximately 23–30% in these boreal bog shrubs (Table 1) compared to the decrease of 80% in boreal and temperate species of Reich, et al. [2]. Thermal acclimation of Rd to temperature increase [1,2,62,66,73,74,75,76] might be a primary interpretation for this finding. However, this study did not find the effects of N and the combined effect of N and W on the response of Rd to CTI in these two bog shrubs (Table 1). These results may be explained by the N fixation capacity of these ericoid shrubs. Unlike other plants, ericoid shrubs can absorb N via symbiotic ericoid mycorrhizal fungi [77,78], therefore, the effects of N addition on these species may be lower than on non-ericoid plants.

4.2. Responses of Net Photosynthesis

The individual effects of eCO2 and/or eT on Anet are well documented. The increases in Anet due to eCO2 have been reported in previous studies [6,11,63,64,79,80]. Also, many recent studies have indicated that temperature increases lead to an improvement of Anet when increases are less than optimal (Topt) [3,81]. In contrast, the rise of temperature reduces Anet if the increases are more than Topt [1,3,62,81,82]. However, the combined effects of eCO2 and eT on Anet are still unclear, with contradictory results reported from recent experiments [8]. The increases [17,83,84,85], no effects [37,86,87,88], or even decrease [37] of Anet due to combined effects of eCO2 and high temperature have been observed.
Our results indicated that CTI decreased Anet in boreal bog vascular plants and Sphagnum moss (Table 2). This finding did not support the hypothesis that CTI would increase Anet in vascular plants. In this study, substantial increases of Rd in the boreal bog plants due to high levels of CTI (C670T3.3 and C936T5.2) may partly explain the decrease in Anet. The reductions in Anet due to CTI in a boreal bog plant were also detected by Ward, et al. [37], which indicated that CTI reduced Anet of C. calyculata by 50% when they examined the combined effects of eCO2 (+500 ppm) and eT (+2–8 °C) on Anet of the species. These findings indicate that high CTI scenarios (RCP6.0 and RCP8.5) may reduce photosynthesis efficiency in existing boreal bog plants, at least in the short term.
We also showed that decreasing levels of Anet due to CTI are species-specific (Table 1). A substantial decrease of Anet in S. fuscum was found at the moderate level of CTI (C538T2.3) (Figure 3j). Meanwhile, declines in Anet were only detected at higher CTI (C670T3.3, C936T5.2) in G. bigeloviana, T. cespitosum (Figure 2i,j and Figure 4i,j), and only at C936T5.2 in A. glaucophylla (Figure 1i,j). These results suggest that S. fuscum is highly sensitive to CTI and the negative effects of eT on the species [30,89,90] may be the main explanation. Being keystone species controlling the growth of other plants as well as vital biochemical processes in boreal bogs [35,91,92,93], the low efficient photosynthesis in Sphagnum under CTI conditions, even in scenarios of moderate CO2 emission (RCP4.5 or C528T2.3 condition), may lead to significant changes in vegetation composition and vital ecosystem services in future.
This research also revealed that long-term N addition regulated the effect of CTI on Anet, wherein the decreases in Anet due to CTI in T. cespitosum were stimulated by N addition during the mid-growing season (Figure 4i, Table 2). The intense stimulation of Rd due to N addition in T. cespitosum (Figure 4g) may partly explain the decrease of Anet in the plant species in the N addition plots (N and NW). In addition, the substantial decrease in soil moisture (Table 3 and Table S1) could be another reason for accelerating the negative effects of CTI on Anet in T. cespitosum in the N addition plots.
We also found that long-term W reduced the adverse effects of CTI on Anet, wherein the decreases in Anet due to high CTI (C936T5.2) in G. bigeloviana in long-term W plots were 93% lower than in control plots during the late-growing season (Figure 2j, Table 2). The thermal acclimation of Anet had been observed in several previous studies [1,74,82,94,95,96]. In this study, the higher Anet in G. bigeloviana at W plots was only detected during the late-growing season (Figure 3j) and not during the mid-growing season (Figure 3i). This finding may indicate that the thermal acclimation of the plant was only effective during the late-growing season. Dry conditions (Figure 2b, Table 3) may be a major limiting factor of the thermal acclimation capacity of G. bigeloviana during the mid-growing season. Decreases in stomatal and mesophyll conductance photosynthesis due to low soil moisture conditions may explain the decrease of Anet [7,97,98,99]. Therefore, dry conditions may erase or limit the thermal acclimation capacity of boreal bog plants [100]. The long-term warmer condition also mitigated the negative effect of long-term N addition on the Anet response of T. cespitosum to CTI during the late-growing season (Figure 4j, Table 2). The thermal acclimation after exposure to a 6-year-W treatment may be a primary reason for this finding.
In this study, we did not examine the specific long-term effects of eCO2 on Rd and Anet responses to CTI. However, there is evidence that long-term exposure to eCO2 reduces the positive effects of short-term eCO2 on Anet [7,11,101,102,103]. Therefore, the decreases in Anet due to CTI may be more considerable under the long-term increases in CO2, temperature, and N-enriched conditions, leading to more severe impacts on boreal bog plants in the future.
This study highlights the crucial roles of long-term N addition and W in regulating responses of Rd and Anet in boreal bog plants to short-term increases in both CO2 and temperatures. However, the intensity and direction effects of long-term W and N addition on boreal bog plant Rd and Anet might depend on levels of these treatments, which have not been shown in this study where the experiment only composited two levels of W (Control vs. ~2 °C) and two two levels of N addition (Control vs. 6.4 gN·m−2·yr−1). Thus, further experiments with multiple levels of these environmental factors are required to determine the potential responses of Rd and Anet in boreal bog plants to the predicted scenarios of atmospheric CO2, temperatures, and N deposition.

5. Conclusions

This study provides evidence that combined increases in CO2 and temperature can increase Rd and reduce Anet in four dominant boreal bog plants, at least in the short term. However, the short-term responses of boreal bog plants to combined increases in CO2 and temperature are regulated by long-term N addition and W treatments. Long-term N addition accelerated the increases in Rd and the decreases in Anet in T. cespitosum; meanwhile, long-term W mitigated the increases in Rd in A. glaucophylla and G. bigeloviana and the decreases in Anet in G. bigeloviana. Although mechanisms that underlie our findings need further studies, we highlight the importance of long-term W and N addition in regulating responses of boreal bog plants to combined increases in CO2 and temperature. Thus, the long-term experiments composited multiple levels of CO2, W, and N addition are required to project the responses of boreal bog plants in the future.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/atmos13101644/s1, Table S1. Summary of models of both CO2 and temperature increments (CTI), warming treatment (W), and N fertilizer addition (N), season, species, and their combined effects on foliar dark respiration (Rd) and net photosynthesis (Anet) in four dominant plant species during the mid and late-growing seasons at a boreal bog. Table S2. Statistical analysis for effects of N addition (N) and warming (W) on environmental variables during the mid-growing season (Mid-season) and late-growing season (Late-season).

Author Contributions

Conceptualization, methodology, T.B.L. and J.W.; formal analysis, investigation, T.B.L.; data curation, T.B.L.; writing—original draft preparation, T.B.L.; writing—review and editing, visualization, T.B.L., J.W., Y.G. and M.-V.D.; Supervision, Project Administration, Funding Acquisition, J.W. All authors have read and agreed to the published version of the manuscript.

Funding

This study was made possible by the support of the following funding to J.W.: Natural Sciences and Engineering Research Council of Canada (NSERC)-Discovery Grant (RGPIN/004466-2016), Canada Foundation for Innovation-John R. Evans Leaders Fund, Research & Development Corporation (RDC, NL)- Leverage R&D, RDC-Ignite R&D, RDC-RCRI (Regional Collaborative Research Initiative), Humber River Basin Research Initiative of NL, Grenfell Campus Research Fund, and the Graduate Student Stipend funding from the Institute for Biodiversity, Ecosystem Science, and Sustainability (IBES, NL). Y.G. and T.B.L. received a Graduate Student Baseline Fellowship from the School of Graduate Studies, Memorial University.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

We appreciate the vegetation identification support from Sveshnikov—Memorial University of Newfoundland, Canada.

Conflicts of Interest

The authors declare no conflict of interest.

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Atmosphere 13 01644 g001 550
Figure 1. The dark respiration (Rd) ((g) for the mid-growing season, (h) for the late-growing season) and net photosynthesis (Anet) ((i) for the mid-growing season, (j) for the late-growing season) of A. glaucophylla in both CO2 and temperature increments (CTI) conditions stimulating future climate scenarios for the year 2100 in the Control (C-red bars), N addition (N-green bars), warming (W-blue bars) and both N addition and warming (NW-purple bars) plots. Error bars represent the standard error of the mean (n = 3). Stars indicate the p-value of the Tukey test for significant differences of Rd and Anet between levels of CTI (*: p < 0.05, **: p < 0.01, ***: p < 0.001). Box plots show environmental variables, including: air temperature (Tair) ((a) for the mid-growing season), (d) for the late-growing season), soil moisture (Msoil) ((b) for the mid-growing season), (e) for the late-growing season), and soil temperature (Tsoil) ((c) for the mid-growing season), (f) for the late-growing season).
Figure 1. The dark respiration (Rd) ((g) for the mid-growing season, (h) for the late-growing season) and net photosynthesis (Anet) ((i) for the mid-growing season, (j) for the late-growing season) of A. glaucophylla in both CO2 and temperature increments (CTI) conditions stimulating future climate scenarios for the year 2100 in the Control (C-red bars), N addition (N-green bars), warming (W-blue bars) and both N addition and warming (NW-purple bars) plots. Error bars represent the standard error of the mean (n = 3). Stars indicate the p-value of the Tukey test for significant differences of Rd and Anet between levels of CTI (*: p < 0.05, **: p < 0.01, ***: p < 0.001). Box plots show environmental variables, including: air temperature (Tair) ((a) for the mid-growing season), (d) for the late-growing season), soil moisture (Msoil) ((b) for the mid-growing season), (e) for the late-growing season), and soil temperature (Tsoil) ((c) for the mid-growing season), (f) for the late-growing season).
Atmosphere 13 01644 g001
Atmosphere 13 01644 g002 550
Figure 2. The dark respiration (Rd) ((g) for the mid-growing season, (h) for the late-growing season) and net photosynthesis (Anet) ((i) for the mid-growing season, (j) for the late-growing season) of G. bigeloviana in both CO2 and temperature increments (CTI) conditions stimulating future climate scenarios for the year 2100 in the Control (C-red bars), N addition (N-green bars), warming (W-blue bars) and both N addition and warming (NW-purple bars) plots. Error bars represent the standard error of the mean (n = 3). Stars indicate the p-value of the Tukey test for significant differences of Rd and Anet between levels of CTI (p < 0.05, **: p < 0.01, ***: p < 0.001). Box plots show environmental variables, including air temperature (Tair) ((a) for the mid-growing season), (d) for the late-growing season), soil moisture (Msoil) ((b) for the mid-growing season), (e) for the late-growing season), and soil temperature (Tsoil) ((c) for the mid-growing season), (f) for the late-growing season).
Figure 2. The dark respiration (Rd) ((g) for the mid-growing season, (h) for the late-growing season) and net photosynthesis (Anet) ((i) for the mid-growing season, (j) for the late-growing season) of G. bigeloviana in both CO2 and temperature increments (CTI) conditions stimulating future climate scenarios for the year 2100 in the Control (C-red bars), N addition (N-green bars), warming (W-blue bars) and both N addition and warming (NW-purple bars) plots. Error bars represent the standard error of the mean (n = 3). Stars indicate the p-value of the Tukey test for significant differences of Rd and Anet between levels of CTI (p < 0.05, **: p < 0.01, ***: p < 0.001). Box plots show environmental variables, including air temperature (Tair) ((a) for the mid-growing season), (d) for the late-growing season), soil moisture (Msoil) ((b) for the mid-growing season), (e) for the late-growing season), and soil temperature (Tsoil) ((c) for the mid-growing season), (f) for the late-growing season).
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Atmosphere 13 01644 g003 550
Figure 3. The dark respiration (Rd) ((g) for the mid-growing season, (h) for the late-growing season) and net photosynthesis (Anet) ((i) for the mid-growing season, (j) for the late-growing season) of S. fuscum in both CO2 and temperature increments (CTI) conditions stimulating future climate scenarios for the year 2100 in the Control (C-red bars), N addition (N-green bars), warming (W-blue bars) and both N addition and warming (NW-purple bars) plots. Error bars represent the standard error of the mean (n = 3). Stars indicate the p-value of the Tukey test for significant differences of Rd and Anet between levels of CTI (p < 0.05, **: p < 0.01, ***: p < 0.001). Box plots show environmental variables, including air temperature (Tair) ((a) for the mid-growing season), (d) for the late-growing season), soil moisture (Msoil) ((b) for the mid-growing season), (e) for the late-growing season), and soil temperature (Tsoil) ((c) for the mid-growing season), (f) for the late-growing season).
Figure 3. The dark respiration (Rd) ((g) for the mid-growing season, (h) for the late-growing season) and net photosynthesis (Anet) ((i) for the mid-growing season, (j) for the late-growing season) of S. fuscum in both CO2 and temperature increments (CTI) conditions stimulating future climate scenarios for the year 2100 in the Control (C-red bars), N addition (N-green bars), warming (W-blue bars) and both N addition and warming (NW-purple bars) plots. Error bars represent the standard error of the mean (n = 3). Stars indicate the p-value of the Tukey test for significant differences of Rd and Anet between levels of CTI (p < 0.05, **: p < 0.01, ***: p < 0.001). Box plots show environmental variables, including air temperature (Tair) ((a) for the mid-growing season), (d) for the late-growing season), soil moisture (Msoil) ((b) for the mid-growing season), (e) for the late-growing season), and soil temperature (Tsoil) ((c) for the mid-growing season), (f) for the late-growing season).
Atmosphere 13 01644 g003
Atmosphere 13 01644 g004 550
Figure 4. The dark respiration (Rd) ((g) for the mid-growing season, (h) for the late-growing season) and net photosynthesis (Anet) ((i) for the mid-growing season, (j) for the late-growing season) of T. cespitosum in both CO2 and temperature increments (CTI) conditions stimulating future climate scenarios for the year 2100 in the Control (C-red bars), N addition (N-green bars), warming (W-blue bars) and both N addition and warming (NW-purple bars) plots. Error bars represent the standard error of the mean (n = 3). Stars indicate the p-value of the Tukey test for significant differences of Rd and Anet between levels of CTI (*: p < 0.05, **: p < 0.01, ***: p < 0.001). Box plots show environmental variables, including air temperature (Tair) ((a) for the mid-growing season), (d) for the late-growing season), soil moisture (Msoil) ((b) for the mid-growing season), (e) for the late-growing season), and soil temperature (Tsoil) ((c) for the mid-growing season), (f) for the late-growing season).
Figure 4. The dark respiration (Rd) ((g) for the mid-growing season, (h) for the late-growing season) and net photosynthesis (Anet) ((i) for the mid-growing season, (j) for the late-growing season) of T. cespitosum in both CO2 and temperature increments (CTI) conditions stimulating future climate scenarios for the year 2100 in the Control (C-red bars), N addition (N-green bars), warming (W-blue bars) and both N addition and warming (NW-purple bars) plots. Error bars represent the standard error of the mean (n = 3). Stars indicate the p-value of the Tukey test for significant differences of Rd and Anet between levels of CTI (*: p < 0.05, **: p < 0.01, ***: p < 0.001). Box plots show environmental variables, including air temperature (Tair) ((a) for the mid-growing season), (d) for the late-growing season), soil moisture (Msoil) ((b) for the mid-growing season), (e) for the late-growing season), and soil temperature (Tsoil) ((c) for the mid-growing season), (f) for the late-growing season).
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Table
Table 1. Summary of models of both CO2 and temperature increments (CTI), warming treatment (W) and N fertilizer addition (N), and their combined effects on dark foliar respiration (Rd) in four dominant plant species during the mid-and late-growing season at a boreal bog.
Table 1. Summary of models of both CO2 and temperature increments (CTI), warming treatment (W) and N fertilizer addition (N), and their combined effects on dark foliar respiration (Rd) in four dominant plant species during the mid-and late-growing season at a boreal bog.
Source of VariationdfRd (µmol·kg −1·s −1)
Mid-Growing SeasonLate-Growing Season
FpFp
Evergreen shrub: A. glaucophylla (n = 60)
CTI491.3<0.0001297.3<0.0001
N10.20.65089.40.0039
W12.10.152010.70.0023
CTI × N41.20.33800.70.6025
CTI × W42.70.04500.20.9565
N × W17.90.00760.30.5716
CTI × N × W40.70.60880.10.9773
Full model adjusted R20.8640.953
Deciduous shrub: G. bigeloviana (n = 60)
CTI477.7<0.0001133.5<0.0001
N12.20.14530.10.8215
W12.20.150622.1<0.0001
CTI × N41.40.25660.30.8771
CTI × W40.80.50884.50.0045
N × W110.60.00241.50.2352
CTI × N × W41.90.12750.70.5943
Full model adjusted R20.8470.907
Sphagnum moss: S. fuscum (n = 60)
CTI444.9<0.000173.5<0.0001
N12.80.10447.40.0099
W11.20.27212.00.1699
CTI × N40.10.99480.20.9194
CTI × W40.10.99290.40.8217
N × W195.8<0.00012.50.1258
CTI × N × W40.10.98270.30.878
Full model adjusted R20.8160.831
Graminoid: T. cespitosum (n = 60)
CTI4229.0<0.000196.4<0.0001
N111.20.001810.00.0031
W11.70.20520.10.7916
CTI × N44.10.00710.20.9551
CTI × W40.50.70300.40.8265
N × W19.60.00377.10.0115
CTI × N × W40.10.97231.70.1766
Full model adjusted R20.9410.870
Table
Table 2. Summary of models of both CO2 and temperature increments (CTI), warming treatment (W), and N fertilizer addition (N), and their combined effects on foliar net photosynthesis (Anet) in four dominant plant species during the mid and late-growing seasons at a boreal bog.
Table 2. Summary of models of both CO2 and temperature increments (CTI), warming treatment (W), and N fertilizer addition (N), and their combined effects on foliar net photosynthesis (Anet) in four dominant plant species during the mid and late-growing seasons at a boreal bog.
Source of VariationdfAnet (µmol·kg−1·s−1)
Mid-Growing SeasonLate-Growing Season
FpFp
Evergreen shrub: A. glaucophylla (n = 60)
CTI48.40.00014.60.0042
N112.20.00133.60.0649
W11.20.27832.60.1153
CTI × N41.90.13270.10.9824
CTI × W40.40.79280.10.9739
N × W10.60.42761.00.3174
CTI × N × W40.00.99780.00.9952
Full model adjusted R20.4290.185
Deciduous shrub: G. bigeloviana (n = 60)
CTI431.7<0.000153.4<0.0001
N134.4<0.00011.60.2097
W11.70.1955114.7<0.0001
CTI × N40.80.56160.70.5983
CTI × W41.20.30933.50.0166
N × W10.80.365827.8<0.0001
CTI × N × W40.10.98531.20.3333
Full model adjusted R20.7510.859
Sphagnum moss: S. fuscum (n = 60)
CTI468.0<0.000156.0<0.0001
N16.80.012916.10.0003
W10.40.52610.70.4037
CTI × N40.10.98161.10.3879
CTI × W40.20.93220.50.7114
N × W1116.2<0.00011.10.3114
CTI × N × W41.20.32941.10.3873
Full model adjusted R20.8670.799
Graminoid: T. cespitosum (n = 60)
CTI499.1<0.000150.3<0.0001
N130.0<0.00012.80.1026
W18.90.00499.70.0035
CTI × N45.30.00172.30.0755
CTI × W42.30.07360.70.5730
N × W10.00.9620.00.8582
CTI × N × W41.10.3884.50.0045
Full model adjusted R20.8890.792
Table
Table 3. Air temperature (Tair), soil moisture (Msoil), and soil temperature (Tsoil) in Control (C), N addition (N), warming (W), both warming and N addition (WN) treatments in the mid-growing season (Mid-season) and late-growing season (Late-season).
Table 3. Air temperature (Tair), soil moisture (Msoil), and soil temperature (Tsoil) in Control (C), N addition (N), warming (W), both warming and N addition (WN) treatments in the mid-growing season (Mid-season) and late-growing season (Late-season).
TreatmentTair (°C)Msoil (%)Tsoil (°C)
Mid-SeasonLate-SeasonMid-SeasonLate-SeasonMid-SeasonLate-Season
C21.63 ± 0.4617.33 ± 0.4336.33 ± 2.9073.60 ± 2.2621.01 ± 0.3617.92 ± 0.61
N21.60 ± 0.4517.40 ± 0.4416.01 ± 1.2064.93 ± 1.9921.43 ± 0.2318.68 ± 0.68
W24.08 ± 0.6819.83 ± 0.6111.18 ± 1.3432.85 ± 1.4724.58 ± 0.4321.23 ± 0.93
WN24.09 ± 0.6619.77 ± 0.6414.11 ± 0.8161.68 ± 1.9023.69 ± 0.3319.95 ± 0.68
Data are presented as mean ± standard error (n = 48).
Table
Table 4. Ammonium (NH4+) and nitrate (NO3−) concentration in soil water at 10 cm and 40 cm depths in control (C), N addition (N), warming (W), and warming and N addition (WN) treatments in the mid-growing season (Mid-season) and late-growing season (Late-season).
Table 4. Ammonium (NH4+) and nitrate (NO3−) concentration in soil water at 10 cm and 40 cm depths in control (C), N addition (N), warming (W), and warming and N addition (WN) treatments in the mid-growing season (Mid-season) and late-growing season (Late-season).
TreatmentNH4+ (mg/L)NO3− (mg/L)
Mid-SeasonLate-SeasonMid-SeasonLate-Season
10 cm depth
C0.366 ± 0.0430.384 ± 0.0800.025 ± 0.0080.190 ± 0.130
N0.982 ± 0.1561.054 ± 0.3550.036 ± 0.0060.511 ± 0.470
W0.454 ± 0.1250.220 ± 0.0630.031 ± 0.0140.056 ± 0.032
WN0.910 ± 0.1781.001 ± 0.2970.090 ± 0.0410.504 ± 0.222
40 cm depth
C0.637 ± 0.1340.642 ± 0.1610.038 ± 0.0110.028 ± 0.010
N1.250 ± 0.1561.087 ± 0.1330.020 ± 0.0070.018 ± 0.003
W0.579 ± 0.0640.680 ± 0.2030.056 ± 0.0190.021 ± 0.006
WN1.127 ± 0.1540.980 ± 0.1420.035 ± 0.0130.020 ± 0.005
Data are presented as mean ± standard error (n = 24).
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Le, T.B.; Wu, J.; Gong, Y.; Dinh, M.-V. Long-Term Warming and Nitrogen Addition Regulate Responses of Dark Respiration and Net Photosynthesis in Boreal Bog Plants to Short-Term Increases in CO2 and Temperature. Atmosphere 2022, 13, 1644. https://doi.org/10.3390/atmos13101644

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Le TB, Wu J, Gong Y, Dinh M-V. Long-Term Warming and Nitrogen Addition Regulate Responses of Dark Respiration and Net Photosynthesis in Boreal Bog Plants to Short-Term Increases in CO2 and Temperature. Atmosphere. 2022; 13(10):1644. https://doi.org/10.3390/atmos13101644

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Le, Thuong Ba, Jianghua Wu, Yu Gong, and Mai-Van Dinh. 2022. "Long-Term Warming and Nitrogen Addition Regulate Responses of Dark Respiration and Net Photosynthesis in Boreal Bog Plants to Short-Term Increases in CO2 and Temperature" Atmosphere 13, no. 10: 1644. https://doi.org/10.3390/atmos13101644

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