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Article

Comparative Ecophysiology of Black Spruce between Lichen Woodlands and Feathermoss Stands in Eastern Canada

by
Catherine Dally-Bélanger
1,2 and
Francois Girard
1,2,*
1
Département de Géographie, Université de Montréal, 1375 Avenue Thérèse-Lavoie-Roux, Montréal, QC H3C 0B3, Canada
2
Centre d’étude de la forêt, Case Postale 8888, Succursale Centre-Ville, Montréal, QC H3C 3P8, Canada
*
Author to whom correspondence should be addressed.
Forests 2022, 13(4), 491; https://doi.org/10.3390/f13040491
Submission received: 27 January 2022 / Revised: 18 March 2022 / Accepted: 21 March 2022 / Published: 22 March 2022
(This article belongs to the Section Forest Ecophysiology and Biology)
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Abstract

:
Climate change is likely to affect the growth, development and regeneration of the black spruce stands across the boreal forest. Regeneration failures cause gaps in the dense black spruce-feathermoss (SM) mosaic increasing the landscape proportion of open lichen woodland (LW). The aims of the study are to determine whether the contrasting characteristics of SM and LW induce different maximum carboxylation rate (Vcmax), maximum electron transport rate (Jmax) and light-saturated maximum photosynthesis (Amax) in black spruce trees across a latitudinal or seasonal gradient. Results show that the Vcmax and Jmax were higher in SM than in LW in western Quebec, at the ecotone of the closed-crown and open forest. Vcmax and Jmax were different between SM and LW mainly because nutrient acquisition seems different between stand types. Latitude affects values of Vcmax and Jmax, but the effect could be explained by soil and vegetation composition between experimental plots rather than by latitude. Physiological capacities do not match Amax values for stand types and latitude. Indeed, Amax rates suggest that black spruce in LWs perform as well as those in SMs at the needle scale because Amax would be limited by CO2 concentration which prevents saturation of Rubisco. Despite the lack of difference between the Amax of SM and LW stands, future increases in CO2 concentration and temperature could induce a gap between their respective photosynthesis rates because of their different physiological capacities.

1. Introduction

In recent decades, dense black spruce feathermoss stands (SM) in the closed-crown forest zone (~47° N to 52° N) have been observed to degrade and/or diverge from the usual ecological trajectory. Dense SMs experience a degradation of their structure evolving into an open stand called lichen woodlands (LW) [1,2,3]. LW stands are commonly found northward, in the open forest zone (~52° N to 55° N). This degradation is linked to successive disturbances (i.e., forest logging, insect epidemics, forest fires), in a short time, which prevent individuals from reaching sexual maturity before the next disturbance [4,5]. The establishment of a viable seed bank is, therefore, compromised, forbidding stand regeneration and the return to its initial state [5,6]. Furthermore, besides the time between two disturbances, the vigor of stressed individuals may limit their reproductive potential [7], creating gaps in the usually dense forest mosaic.
The SM and LW are very contrasting environments in the boreal forest. Their structure and characteristics provide different environments for tree germination and growth. Sphagnum sp. and mosses are widely abundant on the ground of the SM. They promote water and nutrient retention for seedling establishment [8,9,10] and they allow accumulation of organic matter and, thus, of nutrients in the soil [11]. They also protect the roots from frost and limit seasonal fluctuations in soil temperature [12]. The dense forest cover in the SMs promotes a greenhouse effect that stabilizes daily temperature, limiting daytime and nighttime temperature variations compared with the LWs where temperatures can be extreme for trees [13,14]. On the other hand, LWs are a stressful environment for trees [15]. LWs tend to be well-drained soil environments with very little moss or organic matter, which can lead to water stress [2]. Also, the lichen mat on the ground offers a high albedo, which causes large radiative losses [13], lowers the temperature of the soil [13,16], decreases microbial activity [17], slows the decomposition of organic matter [17] and lightens the nutrients available to vascular plants [18,19].
Gas exchange, such as photosynthesis, is useful in determining the effect of environmental conditions on the trees. Photosynthesis allows the tree to obtain the carbohydrates necessary for its growth and reproduction, while being a non-invasive method of measurement [20]. Gas exchange studies can be done at different scales (leaf, tree, stand, ecosystems), which allows estimating tree vigor, stand health, global carbon storage of a forest and to improve global carbon models [21,22,23]. According to the Farquhar-type photosynthesis models [24], the potential photosynthetic capacity of the leaves depends on diffusive (stomatal (gs) and mesophyll (gm) conductance) and non-diffusive factors such as the maximum rate of Rubisco carboxylase activity (Vcmax) and the maximum rate of photosynthetic electron transport (Jmax). Vcmax and Jmax can be obtained from response curves of photosynthesis to intercellular CO2 concentration (Ci), commonly called A–Ci curves. The differences between these Jmax and Vcmax are generally related to the contrasting environmental conditions in which trees grow, such as SM and LW stands. As Vcmax and Jmax represent the potential photosynthetic capacity of a tree, in situ photosynthetic measurements allow the net assimilation rate under ambient or saturating light (Amax) to be determined. Indeed, Amax is dependent on leaf traits (thickness, nutrient concentration, etc.), growing season and vigor.
Little scientific knowledge exists about the gas exchange that occurs in the SM particularly in the LW of eastern Canadian boreal forest at the needle, tree or stand level. A few recent studies investigated the physiological rates and capacities of mature black spruce in SM stands in situ [25,26,27,28], but none focused on LWs, which are often ecosystems north of the attributable forest boundary and, thus, have no commercial interest. Since stand resilience decreases with latitude [3] and increasing temperatures are likely to cause water stress on the black spruce [29], it is necessary to investigate the ecophysiological performance and vigor of the individuals at the northern limit of their bioclimatic domain to assess future changes in biogeography.
The first objective of this study is to determine if the contrasting characteristics between SM and LW result in differences in the maximum photosynthetic rate (Amax) of black spruce at different latitudes and periodicity during the growing season. The second objective is to determine whether the Amax of the individuals reflects their physiological capabilities in terms of maximum carboxylation rate (Vcmax) and maximum electron transport rate (Jmax) by comparing the obtained CO2 response curves. We first hypothesize that individuals in the SMs should have higher Amax, Vcmax, and Jmax than individuals present in the LWs. Indeed, SM provides black spruces a more favorable environment for growth and development (water, temperature, nutrients) [12,13] in comparison with LW where the high albedo of lichens may affect the development of the black spruce [13,16,17]. Second, since forest resilience was shown to decrease with latitude [3], we expect physiological rates and capacities to also decrease with latitude. The photosynthetic rate is expected to increase during the growing season and decrease between August and September [30,31,32], as temperature and photoperiod decrease [31,32,33]. Finally, we suppose that the characteristics of SM and LW at different latitudes should affect photosynthetic rates in the same way as the physiological capacities of individuals and, therefore, the measured Amax values should reflect the physiological capacities of individuals (Vcmax and Jmax).

2. Methods

2.1. Study Area

The study area is in eastern Canada, specifically in western Quebec, in the municipality of James Bay (51–53° N, 77°03′ W). Three latitudes were studied: within the closed-crown forest (51° N), at the ecotone between the closed crown and the open forest (52° N) and within the open forest (53° N) (Figure 1). The elevation of the study area ranges from 190 m to 230 m above sea level. The mean annual temperature is −2.9 °C, while the mean total annual precipitation is 697.2 mm, consisting of 453.8 mm of rain and 261 cm of snow (Environment Canada, 2018). The soil has podzols, but there are also large areas of peatlands in the region. Fire, generally ignited by lightning, is the primary disturbance and all observed forest stands originate from these fires. Stands are, therefore, primarily 120–150 years old, even-aged SM and LW. Commercial logging is not permitted at this latitude and, therefore, does not contribute a significant disturbance in this region. The SM Forest is composed of dense stands where the tree canopy is dominated by black spruce (40% to 100% of the vegetation cover) and the shrub layer is represented by ericaceous species such as Kalmia angustifolia L., Rhododendron groenlandicum (Oeder) Kron & Judd and several species of the genus Vaccinium. The herbaceous stratum, although not very present, is composed of Cornus canadensis L. and Clintonia borealis (Aiton) Raf. and the moss stratum is dominated by Pleurozium schreberi (Willd. ex Brid.) Mitt. and Sphagnum sp. The LW forest is composed of sparsely distributed black spruce occupying only 20% to 40% of the canopy. Its shrub layer is composed of Ericaceae such as Kalmia angustifolia, Chamaedaphne calyculata (L.) Moench and Rhododendron groenlandicum. Its herbaceous layer is almost absent because of the 90–100% ground cover dominated by Cladonia stellaris (Opiz) Pouzar & Vězda.

2.2. Sampling Periods

All data analyzed were collected during a field campaign that took place in three periods of the summer of 2018. The three sampling periods were 21–28 July (mid-July), 30 July–8 August (early August) and 23–29 August (late August). The different sampling dates allowed for the assessment of tree vigor during critical times in the black spruce growing season (shortly after bud break, during the construction of growing and reproductive units and during the consolidation phase).
The first sampling period was determined specifically about the phenology of trees in the study sites. Indeed, a pre-sampling, which took place between 25 and 27 June 2018 to establish experimental plots and observations, showed that black spruce buds were still dormant. Therefore, a period of three weeks from these dates elapsed before measurements could be taken. The beginning of August was the best time to determine the CO2 response curves since this is when the values of the parameters Vcmax and Jmax are generally optimal [34]. Finally, the sampling period at the end of August was chosen because photosynthetic values usually decline at the end of the growing season in favor of reserve consolidation [32]. Depending on the location, this period occurs between August and the end of September in black spruce [30,31,32]. Thus, the last measurement was taken at the end of August to capture the time when photosynthesis begins to decline in the sampled black spruce trees. The sampling period was representative for the study area by considering phenology, climatic conditions and growing season.

2.3. Experimental Design

At each latitude, three pairs of plots were established within a 5 km radius. At all latitudes, each pair consisted of a SM-dominated plot and an LW-dominated plot situated approximately 50 m apart to eliminate microclimatic and edaphic effects from the analysis. Within the 11.28 m radius plots (400 m2), all trees were positioned using a Vertex IV (Haglöf, Torsång, Sweden) then marked with biodegradable forest paint. From these trees, five mature and dominant black spruce trees were randomly selected for measurement, for 80 trees.

2.4. Field Sampling

The annual shoot growth and radial growth of individuals were used as a proxy for their vigor. It was important to select trees with similar vigor to allow comparison of their ecophysiological capacities. Thus, the height and diameter of all the black spruce trees in the experimental plots were measured. During the final field season, in mid-August five to seven twigs between 5 and 17 years old and situated below the reproductive clump of 80 sampled trees were collected. The length of the growth units of each twig was measured in the lab to determine the annual shoot growth over the previous five years. At the end of the field sampling, all 80 sampled trees were cut. A 10 cm-thick disk was taken from the air–soil interface and used to determine the minimum age of the trees by counting the annual radial growth rings. The disks were sanded until the tracheids were visible under a 40× binocular microscope. The thicknesses of the organic and mineral horizons were measured in a pedon (1 m3) that was dug at each plot to determine the nature and structure of the soil. Also, ten holes per plot were systematically dug, each 1 m apart, to determine the average thickness of the organic matter in the plots.
The floristic composition and germination substrates were also characterized in each experimental plot. To do this, the point–intercept method was used to determine the frequency of each species (trees, shrubs, grasses) and soil cover type (woody debris, rock, mineral soil, litter) [35]. This method consisted of four 11.28 m long transects oriented north, south, east and west of the plot centre. At 50 cm intervals, a thin metal rod was placed vertically on the ground to count all individuals and types of ground cover. All individuals having a point of contact with the rod were counted by species and their frequency was determined on all four transects.

2.5. Ecophysiology

All data were collected using the portable photosynthesis measurement system (Model LI-6800, Li-Cor Inc., Lincoln, NE, USA) which uses the Farquahar–von Caemmerer–Berry model to calculate carbon assimilation [24]. Ambient CO2 concentration was measured with the LI-6800 gas exchange module. On a cloudless day, light intensity when the sun was at its peak, solar noon (approximately 1:15 p.m. EDT) was measured with a quantum sensor (Model LI-190R, Li-Cor Inc., Lincoln, NE, USA) installed on the LI-6800 that estimates photosynthetically active radiation (PAR), in μmol of photons s−1 m−2. Using these measurements, a configuration was programmed into the LI-6800 for each type of ecophysiological data measured (Table 1).

2.6. CO2 Response Curves (RACiR)

The RACiR curve method was used since it has many advantages on the quality and quantity of data collected over the traditional A–Ci curve method, while producing comparable results [36]. Indeed, this method is much faster, and the large amount of measured data allows the resolution of the resulting curve to be increased, thereby targeting the inflection points with more precision [36]. Like for the Amax data, measurements for RACiR were taken using the LI-6800 on twigs taken and recut underwater. Measurements were made in early August, when Vcmax and Jmax are at their highest [34].
First, the needles were acclimated to the LI-6800 chamber conditions according to the mentioned parameters (Table 1) at an ambient CO2 concentration of 405 ppm. RACiR and A–Ci curves are usually performed at a temperature of 25 °C, which allows some standardization of the data. However, the ambient temperature when measurements were taken prevented the LI-6800 chamber temperature from being lowered to 25 °C and the RACiR curves were taken at 30 °C. The temperature was measured and controlled by a thermocouple inside the measurement chamber, placed on the abaxial side of the needles. The PPFD was set to 2000 µmol m−2 s−1 to ensure saturation in black spruce was reached [37,38,39]. The relative humidity (50%), fan speed (10,000 rpm), and flow rate (500 µmol mol−1) were the same as in the Amax measurements for the reasons previously discussed. Like the Amax measurements, at the time when photosynthesis was stable (change less than 0.3 µmol m−2 s−1 over a two-minute period), the reference and chamber infrared gas analyzers were matched and automatic data-taking was activated on the LI-6800. The instrument then increased the CO2 concentration to 1500 ppm and then decreased it until the concentration reached 0 ppm over a 10 min period.

2.7. Correction of Ecophysiological Data by Leaf Area

By default, the area used in the calculation of the photosynthetic rate by the LI-6800 is the size of the measurement chamber, i.e., 6 cm2. However, this surface does not correspond to the leaf area of the sampled needles and, therefore, a correction was necessary. Thus, the needles of each sample were digitized using WinSeedle software (version 2005a, Regent Instrument, Quebec City, QC, Canada) and a digitizer (A3F2400N, Mustek, Taiwan). The projected leaf area was used to correct the gas exchange data [25,26,40]. Gas exchange measurements were taken when the needles were fresh, but most leaf areas were calculated from dry needles because needles could not be kept fresh during long field campaigns. During shorter sampling campaigns, fresh samples were also collected and scanned, then dried at 80 °C for 48 h and scanned again. The quotient between the two leaf area measurements was used to apply a correction factor to dry needles. The corrected leaf areas were then associated with the correct measurement in the various Amax data files and RACiR curves using an automated procedure programmed in MatLab (version R2014a).

2.8. Maximum Photosynthetic Rate (Amax)

For each selected individual, a sun-exposed twig was cut using a telescopic pruning saw for measuring gas exchange, including maximum photosynthetic rate (Amax), stomatal conductance (gs), intercellular CO2 concentration (Ci) and transpiration rate (E). Twigs at the top of the tree have higher photosynthetic rates than twigs lower in the tree [25]. The selected twigs had to be exposed to the sun since their chloroplast needles are more efficient than those exposed to the shade [41]. Once the branch was cut, it was immediately placed in a container of water where it was recut underwater using cutters [42,43,44]. Recutting the twigs underwater prevents air from entering the xylem water column during needle transpiration, which breaks the water column and causes a gas embolism [43]. Photosynthesis of twigs that have been re-cut under water usually does not show significant differences from twigs that are still attached to the tree. [42]. To confirm, the original difference was assessed as insignificant when preliminary measurements were taken (results not shown).
Because we wanted the measured Amax values to be representative of the environment in which the sampled black spruce trees were growing, the ambient CO2 concentration (405 ppm) and photosynthetic photon flux density at solar noon (1700 µmol m−2 s−1) were set to match ambient values; when taking measurements, temperature was not controlled to room temperature in the experimental plots. A relative humidity between 40% and 60% is used for ecophysiological measurements in black spruce [45,46,47], therefore an intermediate rate of 50% was used in the present study. The fan speed (10,000 rpm) and the flow rate (500 µmol mol−1) were set according to the LI-6800 recommendations for use to allow for leakage correction and to ensure homogeneous conditions in the measurement chamber.
The needles were acclimated to the chamber parameters and the measurement was taken manually once photosynthesis was stabilized (variation less than 0.3 µmol m−2 s−1 over a two-minute period). Most authors allow a fixed time of 5 min to 10 min for acclimatization of the leaves to the conditions of the measurement chamber [25,32,48]. However, the samples measured in the present study had highly variable acclimation times that could go beyond 15 min. Photosynthesis of the needles increased when placed in a saturating light environment and a change of less than 0.3 µmol m−2 s−1 over a two-minute period showed a stabilization of the photosynthetic curve as a function of time. Once stabilization of photosynthesis was achieved, and if the CO2 and water vapor concentration measured by the two analyzers were different, matching between the reference and chamber infrared gas analyzers was performed before each measurement to apply a correction factor to the point gas exchange measurements.
Measurements were taken from three current-year needle shoots per shoot, except for the early August field season when only one current-year shoot was measured per individual [49]. This is because the battery capacity of the devices was limited, so the amount of data that could be collected from the same collection effort in early August was reduced since the CO2 response curves were also performed at this time. All Amax data were measured between 9:00 and 16:30, i.e., when photosynthetic activity is expected to be maximal in the study area [32,46,50]. The SM and LW plots were also sampled at random on the sampling day to minimize the time-of-day effect. Measurements were also made in the absence of rain and on sunny and cloudy days [32].

3. Data Analysis

The RACiR curves were first corrected with their homologous curve without needles present in the chamber according to the method used by Stinziano, Morgan, Lynch, Saathoff, McDermitt and Hanson [36]. The plantecophys package [51] was then used in R software to analyze the curves and extract the values of Vcmax and Jmax. Like the Amax analysis, a Type III ANOVA was used to test whether there were significant differences between stand types and latitudes and their interaction using R software (version 3.5.3), followed by a Tukey test. To ensure that the values of Vcmax and Jmax were representative of the physiological capacities of the individuals and agree with the measured Amax values, these two parameters were used to extract carbon assimilation (A) values calculated from the RACiR curves. The A values were calculated from the A–Ci function of the plantecophys package. The parameters used in the function were, for each individual, the values of Vcmax and Jmax and the Ci corresponding to that measured during the Amax at the same time as the RACiR curves (beginning of August). The Ci values used corresponded to the Ci when the ambient CO2 concentration was 405 ppm for each individual [25,52]. The calculated A values were compared with the Amax values measured at the same time as the RACiR curves, i.e., in early August, by a paired Student’s t test [53].
Several RACiR curves had to be removed from the analysis since their general appearance and arrangement were not adequate. Indeed, the photosynthetic values of the curves with a needle leaf area of less than 4 cm2 were negative. The overall curve shape appeared adequate. However, it was mostly below the X-axis. The RACiR curves with samples with leaf area greater than 7.4 cm2 were also removed, as these curves had negative Ci values. In total, 51 RACiR curves out of 80 could be analyzed.
For each sampling campaign (mid-July, early August, late August), three Amax values were measured per individual to ensure the validity of these measurements. The three values were then averaged and used to perform the statistical analyses. A linear mixed-effect model was applied to the data. The fixed effects were stand type, latitude, and time in the growing season when the data were taken. The random effects were the experimental plots and the individuals sampled, which allowed for consideration of dependence between data collected on the same plot and individual. A Type III ANOVA (Type III sum of squares) was then performed using R software (version 3.5.3) to test if there were significant differences between different stand types, different latitudes and different times in the growing season. Interactions were also analyzed. Type III ANOVA was used since the experimental design was unbalanced. Indeed, one pair of plots had to be removed from the analysis at latitude 53° N. Subsequent analyses revealed a significantly higher clay content than the other plots, forcing its removal from the experimental protocol. Unfortunately, these plots could not be replaced because of phenological constraints. Indeed, when the soil was analyzed, the advanced phenology of the trees prevented us from establishing a new plot pair to collect new experimental data since the ecophysiological measurements taken at the three latitudes had to be performed in a short time frame. The type III ANOVA analyzes each factor and interaction considering the other factors and interactions of the model, which allows consideration of the unbalanced data [54]. The residuals of the model were subjected to the Shapiro–Wilk normality test and their quantile–quantile diagram was observed to validate their normal distribution. Also, the homogeneity of the variances was observed by plotting the standardized residuals against the fitted values, which showed a random distribution of the standardized residuals around 0. Finally, a Tukey test was then applied to the factors with at least one significantly different level to see which levels were significantly different [55].

4. Results

4.1. CO2 Response Curve

The RACiR curves show that individuals in the SM had a significantly higher potential assimilation rate than individuals in the LW (Figure 2). Indeed, at a Ci of 1200 ppm, individuals in SM had an average photosynthetic rate of 13.6 µmol m−2 s−1 (confidence interval (CI): 11.7–15.5 µmol m−2 s−1), while individuals in LW had an average rate of 9.8 µmol m−2 s−1 (CI: 8.8–10.8 µmol m−2 s−1). SM individuals also had a greater assimilation rate at each Ci measured along the curve compared with LW individuals. The confidence intervals of the RACiR curves by latitude (Figure 2) show that SM and LW individuals appear to have the same potential photosynthetic rate regardless of the latitude at which the data were collected. However, SM individuals from latitude 52° N had the highest average rates.
Vcmax and Jmax extracted from RACiR curves show better physiological capacities for black spruce from SM than from LW (Table 2; Figure 3A,D). SM black spruce had Vcmax rates of 31.5 ± 10.8 µmol m−2 s−1 (mean ± SD) and Jmax rates of 65.9 ± 22.2 µmol m−2 s−1, while LW individuals had rates of 23.5 ± 4.7 µmol m−2 s−1 and 48.3 ± 11.0 µmol m−2 s−1, respectively. Figure 3B,E shows that for both parameters, there is also a significant effect of latitude where Vcmax and Jmax rates were higher at latitude 52° N (32.2 ± 10.9 µmol m−2 s−1 and 66.3 ± 22.6 µmol m−2 s−1, respectively) than at latitude 51° N (23.6 ± 5.1 µmol m−2 s−1 and 47.2 ± 11.9 µmol m−2 s−1, respectively). Individuals at latitude 53° N (24.5 ± 6.5 µmol m−2 s−1 and 53.6 ± 15.1 µmol m−2 s−1, respectively) did not differ from those at the other two latitudes. The significant interaction between stand type and latitude shows that the Vcmax and Jmax rates of individuals from the SM of latitude 52° N are significantly higher than those from the other SM and LW (Figure 3B,E).
Finally, carbon assimilation values (A) calculated from Vcmax and Jmax were not significantly different from Amax values measured at the same time in the growing season (p > 0.05).

Amax

Although SM individuals had a higher physiological capacity than LW individuals, stand type does not appear to affect the net assimilation rate of individuals measured in the field (Table 3). Indeed, the Amax of individuals from SM is 4.7 ± 1.8 µmol m−2 s−1, while that of individuals from LW is 4.4 ± 1.9 µmol m−2 s−1. Furthermore, unlike the Vcmax and Jmax measurements, the Amax measurements did not show a significant difference at the latitudinal level, although it is possible to observe a trend for which the Amax of the SMs from latitude 52° N is slightly higher than the values observed in the SMs and LWs from other latitudes.
Amax increased significantly during the growing season (Table 3; Figure 4), ranging from 2.9 ± 1.2 µmol m−2 s−1 in mid-July to 4.7 ± 1.4 µmol m−2 s−1 in early August and finally 6.2 ± 1.2 µmol m−2 s−1 in late August. The ambient temperature on the experimental plots during the measurements was inversely proportional to the Amax values (Figure 5B). Indeed, the ambient temperature decreased significantly during the growing season (Table 3; Figure 5A). It, thus, varied from 33.0 ± 3.2 °C in mid-July, to 27.4 ± 2.9 °C in early August and finally to 21.3 ± 3.7 °C at the end of August. According to Figure 5B, Amax values were optimal when the ambient temperature was approximately 20 °C and they decreased when the temperature was above 25 °C. The stomatal conductance followed the same pattern as Amax, i.e., it increased during the growing season (Table 3). It is 0.053 ± 0.021 mol m−2 s−1 in mid-July, 0.070 ± 0.036 mol m−2 s−1 in early August, and finally 0.093 ± 0.048 mol m−2 s−1 in late August.
The significant interaction between latitude and time in the growing season shows that there are significant differences between some latitudes at certain times in the growing season (Figure 6). However, the time of the growing season had the same effect on Amax values at each of the latitudes studied since there is no difference between latitudes for the same time of the season.

5. Discussion

In the literature, black spruce Vcmax and Jmax rates were measured using the traditional method of A–Ci curves and the authors obtained an average Vcmax rate between 15 and 60 µmol m−2 s−1 and average Jmax rates between 34 and 225 µmol m−2 s−1 [25,34,38,56]. To our knowledge, only one study has used traditional and RACiR methods together for black spruce, obtaining similar results between the two methods and Vcmax and Jmax values of 62 and 119 µmol m−2 s−1, respectively [48]. The values measured in our study were similar to the rates found in studies performed using the traditional method. On the other hand, they were significantly lower than values obtained with the RACiR method, probably due to the environment and age of the seedlings used by Coursolle, Otis Prud’Homme, Lamothe and Isabel [48]. Moreover, there appears to have a great variability in the Vcmax and Jmax of black spruce across studies that used the traditional method.
The photosynthetic rates (Amax) of black spruce measured in this study resemble the rates found in the literature for similar measurement parameters (saturating light, CO2 concentration of about 400 ppm, temperature between 20 and 30 °C, leaf area evaluated by the projected area method). Indeed, the average photosynthetic rate of those studies varied between 2.6 and 12 µmol m−2 s−1 [25,26,56]. The majority of studies with Amax values on black spruce were conducted in SM stands or in greenhouses and only one was conducted in environments like that of western Quebec LW [57]. All values, including the present study, were calculated from the Farquhar, von Caemmerer and Berry [24], which implies that the parameters are comparable and have been calculated from the same equations.

5.1. Differences between SM and LW

The contrast in environments between SM and LW was distinctly seen in the rates of Vcmax and Jmax measured in this study. Indeed, the LW and SM rates were significantly different, being higher in the SM. Several factors may influence the measured Vcmax and Jmax rates. Among them, the nitrogen available in the soil [50,52,58], the optimal tree growth temperature [56,59] and light intensity [60,61] are the variables that appear to have the greatest influence on the physiological capacities of the trees. To a lesser extent, soil moisture and relative air humidity can also affect Vcmax and Jmax [59].
The organic layer of the soil and the effect of lichens on the symbiotic associations of the roots with ectomycorrhizae may explain the observed differences between the physiological capacities of the trees composing the SM and the LW. First, since black spruce roots are located in the top few centimeters of soil [62,63], a thin organic matter layer found in the LWs could be hostile for black spruce. Indeed, the nutrient supply differs along with the increasing thickness of the organic matter [64]. Since the litter and the soil of the boreal forest are cold and acidic, decomposition by microorganisms is slow and nutrient availability is limiting [65,66]. Indeed, authors reported positive correlations between the leaf nitrogen and the rates of Vcmax and Jmax, even for black spruce [50,52,58,59,61]. Foliar nitrogen was not measured in this experiment because literature has shown no difference in foliar nitrogen between trees in SM and LW [49,67]. Soil leachate from lichens also alters the composition and abundance of ectomycorrhizae on the surface of tree roots, thereby limiting their nutrient uptake [11,68]. These fungi normally stimulate tree growth in nutrient-poor soils by binding to their roots to transfer nutrients from the soil organic matter [69]. Thus, the acquisition of the black spruce may be compromised in LW and lead to lower Vcmax and Jmax rates. A thorough study of nutrient uptake in both LW and SM is needed to investigate further.
Soil moisture and relative air humidity were not measured on the experimental plots, as the latter was controlled in the measurement chamber. The thick layer of organic matter found in the SM favors a higher soil moisture and the greenhouse effect of the forest cover could allow a higher relative humidity than in the LW and favor higher Vcmax and Jmax rates. Amax data collected over the growing season show no significant difference in stomatal conductance (gs) for stand type, suggesting that stomata have the same constraint on opening whether individuals are in a SM or LW. Indeed, water vapor deficits and water stresses that trees may experience cause stomata to close and thus reduce gs [70,71,72]. However, relative humidity in the measurement chamber was the same for both LW and SM gas exchange measurements and since it influences stomatal opening, it is not surprising that there was no effect of stand type on gs. Even under water stress, gs does not necessarily decrease in black spruce [73] and it would, therefore, be preferable to take potential water measurements to investigate the water status of the trees.
Contrary to what was expected, the physiological capacities (Vcmax and Jmax) of black spruce are not reflected in the photosynthetic rate measured directly in the field (Amax). This, therefore, implies that despite fundamental differences in tree physiology, black spruce in SM and LW have the same needle-scale yield. Tremblay, Boucher, Tremblay and Lord [57] also observed no difference between black spruce Amax in SM and LW.
Several environmental conditions can influence Amax, such as ambient temperature [60,74], light intensity [60,75], air humidity [76,77], frost [38,74] and soil hydric potential [72,78]. The ambient temperature, light intensity and relative air humidity were controlled in the measurement chamber and, therefore, should not be a factor that influences the measured Amax. As for Jmax and Vcmax, nitrogen is also an important factor. For black spruce, nitrogen availability has been observed to favor Amax [40,50,52], or sometimes has no remarkable effect [28,39,57,79]. The consensus on nitrogen is not unanimous since fertilization treatments from different studies have given different results on Amax values. However, nitrogen could affect Jmax rates up to twenty-two times more and Vcmax rates up to eight times more than Amax [52]. If there would be a greater availability of nitrogen in the SM soil and its acquisition would be different between the two stands, it would be likely that the nitrogen in the soil and in the needles of the trees would affect the physiological abilities of the individuals but would not be reflected in the rate of photosynthesis measured in the field.
The ambient CO2 concentration regulates the values of Amax. Indeed, the average Ci measured in black spruce and corresponding to an ambient concentration of 405 ppm CO2 is well before the first inflection point of the RACiR curves. Before this inflection point, the limiting element of photosynthesis is the capacity of the Rubisco enzyme to use CO2 to carboxylate RuBP molecules (Vcmax) because the intercellular CO2 is not large enough to carboxylate all available RuBP molecules [60,80]. Thus, there would not be enough atmospheric CO2 to saturate the enzyme Rubisco [81] and that a difference in Amax can be observed regardless of the thickness of the organic matter and mycorrhizal associations of the roots. This trend is also observed in other species adapted to cold environments [82,83]. The results of this study also remind us that the supply of carbon via photosynthesis, even stressed, is a high priority for trees. Indeed, the assimilated carbon can then be reinvested in the maintenance and repair of the photosynthetic apparatus [84] or in the roots to increase access to resources (water, nutrients) [85].
This mismatch between the physiological capabilities of black spruce and their Amax could have medium to long-term effects on climate change. LWs will likely become increasingly stressed environments with changing precipitation patterns and increasing temperatures. Also, the increase in atmospheric CO2 concentration may amplify the potential discrepancy between SM and LW since the Rubisco enzyme will be able to carboxylate more RuBP molecules in SM, but will be limited in LW, due to the lower physiological capacity of the individuals. For now, the characteristics of the LWs do not affect the photosynthesis of the trees measured in situ, but it will be important to monitor any ecophysiological changes that may occur between the SM and LWs to ensure the continuity of knowledge in the black spruce forests of eastern Canada.

5.2. Latitude

In eastern Canada, the number of degree days, average annual temperatures, maximum and minimum temperatures and precipitation tends to decrease with latitude [86]. Over the 300 km latitudinal gradient between experimental plots (51° N, 52° N, 53° N), the mean, minimum and maximum annual temperatures vary by about 1.5 °C, 1 °C and 2 °C, respectively [86]. The observed differences in Vcmax, Jmax and Amax are not related to latitude but to site characteristics. The results of this study demonstrate that photosynthetic differences may exist over larger latitudinal gradients than were assessed in this study and that at the scale at which the data were collected, environmental conditions at the study sites do not have a large enough effect to make the Amax data different at the latitudes sampled. This also demonstrates the great plasticity of black spruce, whose stands extend from the Great Lakes region (43° N) to the beginning of the permafrost (56–58° N). The physiological plasticity of the species, thus, largely exceeds the small climatic variations of the latitudes studied. A few studies evaluated the ecophysiology of black spruce across a latitudinal gradient and their results were divergent. Johnsen, Seiler and Major [30] observed that black spruce in the Yukon (63° N) have higher photosynthetic rates than their Ontario counterparts (45° N) in June and July, but that the opposite trend was be observed in September and October, when the growing season is over in the Yukon, but continues in Ontario.

5.3. Growth Season

During the growing season, the phenology of Amax is mainly related to the photoperiod [30,32,33] and at ambient temperature [31,32,87]. Photosynthesis increases as spring temperatures rise [74] and decreases in autumn with the arrival of cooler temperatures which accentuate the effect of the photoperiod [38]. In black spruce, great variability exists in the phenology of Amax and the attainment of its maximum value and the onset of its decline. The end of photosynthesis does not appear to be linear with the latitude in which studies are conducted. As the physiological stage of these growing needles evolves, the concentration of nitrogen, carbon, and chlorophyll, and the capacity of the Rubisco enzyme, increases over the course of the summer, until these needles are mature [88]. This improves their photosynthetic apparatus and increases their photosynthetic rate [39].
The ambient temperature of the experimental plots at the time the measurements were taken is strongly correlated with the Amax values. The decrease in temperature between mid-July and the end of August seems to favor higher photosynthetic rates in late summer. Indeed, when the ambient temperature is above 25 °C, as was the case in mid-July, photosynthesis of trees peaks, stabilizes, then decreases. For black spruce, this temperature corresponds to the thermal limit of the photosynthetic optimum: Amax remains at 90% of its maximum value between 15 °C and 25 °C [31,56,89]. Higher temperatures force the closure of stomata to limit water loss by evapotranspiration, thus limiting the entry of CO2 necessary for photosynthesis.

6. Conclusions

Results show that the maximum carboxylation rate (Vcmax) and maximum electron transport rate (Jmax) were higher in SM than in LW in western Quebec, at the ecotone of the closed-crown and open forest. Differences between SM and LW, therefore, affected the physiological capabilities of individuals. These rates also differed between the latitudes sampled, but only SM at 52° N latitude differed from the other experimental plots, suggesting that plot-specific conditions influenced Vcmax and Jmax rates more than latitude per se. Contrary to our hypothesis, the physiological capabilities of black spruce were not reflected in the maximum photosynthetic rate at saturating light (Amax). The current atmospheric CO2 concentration prevents the first inflection point of the CO2 response curves to be reached, thus the Rubisco enzyme does not reach its saturation threshold and is, therefore, not limiting for photosynthetic processes. The black spruce sampled would, therefore, have similar photosynthetic rates regardless of the stand type or latitude at which they grow. Despite the differences in physiological capacities, the in situ photosynthetic rate suggests that black spruce in LWs perform as well as those in SMs at the needle scale.
The data in this study are from a single year of observations and, therefore, additional years of physiological measurements are needed to obtain an adequate picture of the physiology of individuals in the study area [34]. Furthermore, with increasing atmospheric CO2 concentration, it can be expected that the gap between the Amax of SM and LWs will widen. With a higher concentration of CO2, the diffusion of CO2 inside the needles is greater and, therefore, more CO2 molecules can be used for the carboxylation of RuBP molecules and thus, the saturation of the Rubisco enzyme [90]. On the other hand, the physiological capacities (Vcmax and Jmax) of black spruce tend to decrease when the CO2 concentration increases above 600 ppm [38,91] as the amount and/or activation of the Rubisco enzyme decreases [90]. Other ecophysiological studies will be essential in the years to come, particularly in northern ecosystems where climate change will be more significant.

Author Contributions

The conception, design and methodology implementation were undertaken by C.D.-B. and F.G.; experiment execution, data analysis/interpretation and data collection were realized by C.D.-B. Finally, manuscript writing/revision was undertaken by F.G. and C.D.-B. All authors have read and agreed to the published version of the manuscript.

Funding

This research was supported by the Natural Sciences and Engineering Research Council of Canada (NSERC), grant: 04861-2016.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data available upon request to authors.

Acknowledgments

For field assistance, Marie-Claude McDuff, Patricia Girardin and Simon Charbonneau are gratefully acknowledged. We also acknowledge two anonymous reviewers for their relevant comments on an earlier version of the manuscript.

Conflicts of Interest

The authors declare no conflict of interest.

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Forests 13 00491 g001 550
Figure 1. Study area and localization of the experimental plots in the boreal forest of eastern Canada.
Figure 1. Study area and localization of the experimental plots in the boreal forest of eastern Canada.
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Forests 13 00491 g002 550
Figure 2. RACiR curves of SM and LW averaged for all latitudes (A) and LW and SM along a latitudinal gradient ((B,C), respectively). Colored areas represent 95% confidence intervals, and the dashed line represents the mean Ci at ambient CO2 concentration (405 ppm).
Figure 2. RACiR curves of SM and LW averaged for all latitudes (A) and LW and SM along a latitudinal gradient ((B,C), respectively). Colored areas represent 95% confidence intervals, and the dashed line represents the mean Ci at ambient CO2 concentration (405 ppm).
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Forests 13 00491 g003 550
Figure 3. Maximum Rubisco carboxylation rate (Vcmax, (A–C)) and maximum electron transport rate (Jmax, (D–F)) averaged for trees in SMs and LWs for all latitudes (A,D), the different latitudes sampled (B,E), and the interaction between stand type and latitude (C,F). Solid points and letters represent the mean and significant differences from the 5% level (Tukey test), respectively.
Figure 3. Maximum Rubisco carboxylation rate (Vcmax, (A–C)) and maximum electron transport rate (Jmax, (D–F)) averaged for trees in SMs and LWs for all latitudes (A,D), the different latitudes sampled (B,E), and the interaction between stand type and latitude (C,F). Solid points and letters represent the mean and significant differences from the 5% level (Tukey test), respectively.
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Figure 4. Evolution of Amax during the growing season. Solid points and letters represent, respectively, the mean and the significant differences from the 5% threshold (Tukey test).
Figure 4. Evolution of Amax during the growing season. Solid points and letters represent, respectively, the mean and the significant differences from the 5% threshold (Tukey test).
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Figure 5. Changes in ambient temperature on the experimental plots during the growing season (A) and relationship between maximum photosynthetic rate (Amax) and temperature (B). Points and letters (A) represent means and significant differences from the 5% level (Tukey test), respectively.
Figure 5. Changes in ambient temperature on the experimental plots during the growing season (A) and relationship between maximum photosynthetic rate (Amax) and temperature (B). Points and letters (A) represent means and significant differences from the 5% level (Tukey test), respectively.
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Figure 6. Interaction between Amax values for latitude and time in the growing season. Solid points represent the mean and letters represent significant differences at the 5% level between latitude and time of growing season (Tukey test).
Figure 6. Interaction between Amax values for latitude and time in the growing season. Solid points represent the mean and letters represent significant differences at the 5% level between latitude and time of growing season (Tukey test).
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Table
Table 1. Configuration of the LI-6800 when taking data for ecophysiological measurements. [CO2]: CO2 concentration; RH: relative humidity; PPFD: photosynthetic photon flux density, Tneedle: temperature of sampled needles.
Table 1. Configuration of the LI-6800 when taking data for ecophysiological measurements. [CO2]: CO2 concentration; RH: relative humidity; PPFD: photosynthetic photon flux density, Tneedle: temperature of sampled needles.
Measurements[CO2] RHPPFDTneedleFanFlow
(ppm)(%)(µmol m−2 s−1)(°C)(rpm)(µmol mol−1)
AmaxAmbient 40550Ambient and saturating 1700Ambient Uncontrolled10,000500
RACiRVariable 0–150050Saturating 20003010,000500
Table
Table 2. Summary of ANOVA result (chi-square and p-value) of carboxylation (Vcmax) and electron transport (Jmax) rates. Bolded p-value indicates a significant difference at the 5% threshold.
Table 2. Summary of ANOVA result (chi-square and p-value) of carboxylation (Vcmax) and electron transport (Jmax) rates. Bolded p-value indicates a significant difference at the 5% threshold.
FactorsVcmaxJmax
χ2p-Valueχ2p-Value
Type of stand6.450.0117.850.005
Latitude8.260.0167.310.026
Type: Latitude7.040.0304.430.109
Table
Table 3. Summary of ANOVA result (chi-square and p-value) of maximum photosynthetic rates (Amax), water vapor stomatal conductance (gs), and ambient temperature at the time of measurement (Tambient). Bold p-value indicates significant difference at the 5% threshold.
Table 3. Summary of ANOVA result (chi-square and p-value) of maximum photosynthetic rates (Amax), water vapor stomatal conductance (gs), and ambient temperature at the time of measurement (Tambient). Bold p-value indicates significant difference at the 5% threshold.
FactorsAmaxgsTambient
χ2p-Valueχ2p-Valueχ2p-Value
Type of stand0.640.4241.820.1780.530.465
Latitude0.910.6340.790.6750.090.958
Growth season347.87<0.00142.13<0.0012114.40<0.001
Type: Latitude5.070.0790.010.9980.200.904
Type: Season1.250.5353.900.14218.41<0.001
Latitude: Season14.560.0064.750.313122.17<0.001
Type: Latitude: Season2.600.6261.030.9057.640.106
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Dally-Bélanger, C.; Girard, F. Comparative Ecophysiology of Black Spruce between Lichen Woodlands and Feathermoss Stands in Eastern Canada. Forests 2022, 13, 491. https://doi.org/10.3390/f13040491

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Dally-Bélanger C, Girard F. Comparative Ecophysiology of Black Spruce between Lichen Woodlands and Feathermoss Stands in Eastern Canada. Forests. 2022; 13(4):491. https://doi.org/10.3390/f13040491

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Dally-Bélanger, Catherine, and Francois Girard. 2022. "Comparative Ecophysiology of Black Spruce between Lichen Woodlands and Feathermoss Stands in Eastern Canada" Forests 13, no. 4: 491. https://doi.org/10.3390/f13040491

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