Diurnal, Seasonal, and Vertical Changes in Photosynthetic Rates in Cinamomum camphora Forests in Subtropical China

Forests actively sequester atmospheric carbon dioxide through photosynthesis and play a vital role in offsetting anthropogenic carbon emissions and mitigating climate change [1]. Over the past two decades, there has been a growing worldwide concern regarding the rise in greenhouse gases and their potential impacts on global environmental change [2]. CO₂ stands as a major greenhouse gas and plays a pivotal role in global warming [3]. Due to the extensive coverage of forests across the planet, the study of CO₂ flux, carbon balance, and net productivity within forest ecosystems has become a central focus of research in the field of forest ecosystems [4,5]. It is widely recognized that photosynthesis is a crucial mechanism for removing CO₂ from the atmosphere and storing it in the biosphere [6,7]. Therefore, understanding the photosynthetic characteristics of individual tree species and various forest ecosystems has become of imperative importance [8,9].

Photosynthesis is the process through which green plants capture solar energy and use it to convert carbon dioxide and water into reduced carbon compounds [10]. It stands as the most significant CO₂ flux within forest ecosystems and is the biological mechanism responsible for carbon sequestration by forests. Remarkably, it is estimated that photosynthetic organisms fix approximately 1.0 × 10¹⁴ kg of carbon into organic compounds annually. To put this in perspective, this amount is equivalent to about 1% of the world’s known reserves of fossil fuels, including coal, gas, and oil, or roughly 10 times the world’s current annual energy consumption [11]. Canopy photosynthetic productivity serves as the primary driver for promoting and sustaining forest formation and serves as the primary energy source for canopy carbon supply and metabolism [12,13]. The vertical distribution of the canopy directly influences trees’ photosynthetic capacity and growth [14], consequently impacting the overall performance and productivity of the entire forest stand [15,16,17]. This dependence on photosynthetic productivity stems from the complex interplay of factors, including the three-dimensional forest stand structure, canopy leaf photosynthetic capacity, and the efficiency of light interception and conversion under specific environmental conditions [18,19,20]. Understanding the influence of canopy vertical distribution on photosynthetic productivity is crucial for comprehending forest productivity formation and enhancing the ecosystem’s carbon sequestration capacity [21]. Therefore, it is important to develop forest management strategies and investigate forest productivity from an ecological and physiological perspective [22,23].

Significant variations exist in the vertical distribution of light within the layers of the forest canopy [24,25]. The light environment in forests varies significantly based on stand age, species composition, and stand structure [26]. For instance, in young forest stands, relative light intensity does not consistently decrease from the top to the bottom due to incomplete canopy closure and the presence of gaps between neighboring trees, allowing light to enter from various angles, not just from above [27]. In old Douglas fir trees, a local light intensity peak occurs near the middle canopy because of the lateral penetration of diffused light [19,24,25]. The utilization of forest light energy is influenced by the vertical distribution of the canopy [28]. Photosynthetic rates exhibited variability across canopy layers; in oak trees, the net assimilation of lower canopy leaves underwent a more significant decrease compared to sunlit leaves on the upper canopy [29]. Numerous studies have been conducted to examine the photosynthetic characteristics of selected tree species within evergreen broad-leaved forests in subtropical regions. For example, studies investigated the photosynthetic properties of two key tree species, evergreen Chinkapin (Castanopsis fissa) and Guger tree (Schima superba gardn), in the subtropical region under varying CO₂ concentrations [30]. The findings revealed that, compared to values under 350 μmol mol⁻¹ CO₂, the photosynthetic rates of these species increased by 79% and 95%, respectively, under 500 μmol mol⁻¹ CO₂. In a separate study, light saturation points ranging from 1000 to 1900 μmol m⁻² s⁻¹ of photosynthetically active radiation (PAR), light compensation points ranging from 4.8 to 30.1 μmol m⁻² s⁻¹ of PAR, and a maximum photosynthetic rate of 13.3 μmol CO₂ m⁻² s⁻¹ for mature Chinese fir were reported [31].

The environmental conditions, specifically the contrast between cloudy and sunny conditions, along with seasonal variations, play a crucial role in influencing the rate of photosynthesis. Numerous studies have explored the intricate interplay between light intensity, temperature, and atmospheric conditions on photosynthetic processes. Furthermore, the impact of seasonal changes, such as variations in temperature and day length, can significantly alter the overall photosynthetic activity of plants. For instance, a more even distribution of light among leaves across the vertical profile of the canopy is considered the most important factor contributing to this difference [32]. The cloud cover had a significant impact on carbon exchange between the biota and the atmosphere and an increase in the fraction of diffuse radiation enhances the photosynthetic efficiency of canopies [32]. A study reported that all physiological observations were 2–3 times lower under cloudy conditions in the rainy season [33]. However, an observation found that on a daily timescale, Net ecosystem productivity (NEP) and gross primary production (GPP) were higher under both cloudy and sunny conditions compared to overcast conditions across seasons. Specifically, the daily NEP and GPP during the wet season peaked under cloudy skies [34]. Studies have demonstrated that net photosynthetic rates decline rapidly as temperatures increase above the optimal temperature [35,36]. Seasonal temperature changes also affected net photosynthetic rates; net photosynthetic rates were highest in spring and autumn, and lowest in July, August, and December–January in Douglas Fir Seedlings [37].

As a native species in China, the Camphor tree (Cinnamomum camphora (L.) J. Presl) is an evergreen broadleaf tree species widely distributed in tropical and subtropical regions of the nation, with a history of exploitation and utilization spanning over a thousand years [38]. Characterized by relatively fast growth, high-quality timber, and abundant camphor oil production, the Camphor tree has been cultivated for various purposes, including timber, medicine, pesticides, and ornamental use. In addition, Camphor tree forests have been managed for urban landscaping, carbon sequestration, and ecosystem services, such as soil and water conservation, owing to their dense canopy, richness of fallen leaves, large biomass, and flourishing root systems [39]. Due to these attributes, the Camphor tree is regarded as a representative and valuable species in evergreen broadleaf forests, which constitute the typical climax forest community in subtropical regions of China [38,40]. These forests play a critical role in biodiversity conservation, regulating essential local ecological processes like energy flow, water balance, and nutrient cycling. Furthermore, they contribute significantly to the maintenance of regional landscape ecosystems in the subtropical zone [39,40]. However, despite their ecological importance, the photosynthetic characteristics of Camphor tree forests in subtropical zones remain poorly understood. Less is known about the dynamics of the photosynthesis process in Camphor tree forests. This information is crucial for gaining insights into the carbon sequestration potential of Camphor forests.

Figure 2 displayed the overall average of photosynthetic rates during both sunny and cloudy days, as well as the seasonal pattern. On average, the photosynthetic rate was marginally significantly higher on sunny days than on cloudy days (p = 0.055) (Figure 2b). The maximum rate of photosynthesis recorded was 18.9 µmol CO₂ m⁻² s⁻¹ for sunny days and 13.2 µmol CO₂ m⁻² s⁻¹ for cloudy days. Additionally, the diurnal pattern of the photosynthesis process on cloudy days exhibited significant differences from that on sunny days.

On sunny days, the rate of photosynthesis exhibited a characteristic pattern, with an increase in the morning followed by a decline in the afternoon (Figure 2a). This diurnal variation was consistent throughout the growing season, spanning from May to October, and featured a distinct midday depression in photosynthesis around 13:00 h. Particularly, photosynthesis displayed two peaks, with the first occurring around 12:00 noon and the second around 14:00 h (Figure 2a). The maximum rates of photosynthesis for each month were as follows: May (10.1 µmol CO₂ m⁻² s⁻¹), June (18.9 µmol CO₂ m⁻² s⁻¹), July (10.5 µmol CO₂ m⁻² s⁻¹), August (8.1 µmol CO₂ m⁻² s⁻¹), September (15.9 µmol CO₂ m⁻² s⁻¹), and October (10.3 µmol CO₂ m⁻² s⁻¹). Notably, the values measured between 9:00 and 10:00 h and between 15:00 and 16:00 h closely approximated the daily average photosynthetic rate, as calculated from the hourly measurements taken between 8:00 and 18:00 h. Furthermore, photosynthetic production during the peak periods (10:00 to 12:00 h and 14:00 to 16:00 h) accounted for approximately 80% of the total daily photosynthetic production observed between 8:00 and 18:00 h. Cloudy days lacked the midday depression typically observed in photosynthesis, displaying only one peak occurring around 12:00 noon (Figure 2b). Interestingly, photosynthesis on cloudy days still followed a morning increase and an afternoon decrease, resembling the general pattern of photosynthesis observed on sunny days (Figure 2a,b). The daily average rate of photosynthesis on cloudy days amounted to approximately 74% of that on sunny days.

Photosynthetic rates were significantly higher in the upper and middle canopy layers than in the lower canopy layer (p Figure 2c). Specifically, the upper canopy layers exhibited higher photosynthetic rates than the middle canopy layer, although no significant differences were found between these two canopy layers (p > 0.05).

The maximum rates of photosynthesis recorded were 18.9 µmol CO₂ m⁻² s⁻¹ for the upper canopy, 15.9 µmol CO₂ m⁻² s⁻¹ for the middle canopy, and 4.7 µmol CO₂ m⁻² s⁻¹ for the lower canopy. Furthermore, the daily average rate of photosynthesis in the middle and lower canopies amounted to approximately 83% and 25% of that observed in the upper canopy, respectively. The diurnal patterns of photosynthesis exhibited notable differences among different canopy layers. Specifically, the upper and middle canopy layers displayed similar patterns, as previously described, with distinct peaks and a midday depression (Figure 2c). However, the photosynthesis of leaves in the lower canopy layer presented a distinct pattern, devoid of obvious peaks or midday depression (Figure 1c). Between 9:00 and 15:00 h, there were minimal variations in the rate of photosynthesis in the lower canopy, whereas an increasing trend was observed between 8:00 and 9:00 h, followed by a decreasing trend between 15:00 and 18:00 h (Figure 2c).

The upper canopy displayed the highest PAR-saturated rate of net photosynthesis, which was significantly higher than that in the middle and lower canopy layers (p Figure 3). In the lower canopy, photosynthesis began to decline as PAR levels increased, particularly in the range of 300 to 400 µmol m⁻² s⁻¹. Conversely, the middle canopy started to experience a decrease in photosynthesis at higher PAR levels, typically around 700 to 800 µmol m⁻² s⁻¹. Intriguingly, the photosynthesis of leaves in the upper canopy layer remained unaffected by increasing PAR until it exceeded 1200 µmol m⁻² s⁻¹. Furthermore, the light compensation points were measured at 95, 67, and 31 µmol m⁻² s⁻¹ PAR for the upper, middle, and lower canopy layers, respectively. The rates of dark respiration derived from the PAR response curve were found to be 1.73 µmol m⁻² s⁻¹ for the upper canopy, 1.25 µmol m⁻² s⁻¹ for the middle canopy, and 1.0 µmol m⁻² s⁻¹ for the lower canopy layer. Additionally, the apparent quantum yield of photosynthesis was calculated as 0.0183 µmol CO₂ µmol⁻¹ PAR for the upper canopy, 0.0186 µmol CO₂ µmol⁻¹ PAR for the middle canopy, and 0.0327 µmol CO₂ µmol⁻¹ PAR for the lower canopy (Figure 3). Interestingly, the mean photosynthetic rate was significantly higher in the upper canopy than in the middle and lower canopy layers, but under the 300 to 400 µmol m⁻² s⁻¹ of PAR, the photosynthetic rates in the middle and lower canopy layers exceed that in the upper canopy layer (Figure 3).

Among the different canopy positions, the upper canopy consistently exhibited the highest photosynthesis rate, while the lower canopy consistently displayed the lowest, except under very low CO₂ concentrations (Figure 4). On average, photosynthesis rates were significantly higher in the upper canopy layer than in the lower canopy layer (p p > 0.05). The CO₂ compensation points were found to be 52 µmol mol⁻¹ for the upper, 51 µmol mol⁻¹ for the middle, and 52 µmol mol⁻¹ for the lower canopy layer. Additionally, the initial slope of the response curve was calculated as 0.0354 mol m⁻² s⁻¹ for the upper canopy, 0.0186 mol m⁻² s⁻¹ for the middle canopy, and 0.0144 mol m⁻² s⁻¹ for the lower canopy.

Photosynthesis rates exhibited significant seasonal variations throughout the growing season. Peaks in photosynthesis were observed during two distinct periods in June and September, with considerably lower rates during non-peak periods (Figure 5). In particular, the peak photosynthesis rates in June generally surpassed those recorded in September. While leaves in different canopy layers displayed similar seasonal patterns, the magnitude of variation in the lower canopy layer was notably smaller compared to the upper and middle canopy layers (Figure 5). On average, monthly photosynthesis rates were significantly higher in the upper and middle canopy layers than in the lower canopy layers (p ⁻¹ and 71.6 t C ha⁻¹, respectively.

This study highlights that the diurnal patterns of net photosynthesis remained consistent throughout the growing season, spanning from May to October. However, these patterns exhibited variations dependent on weather conditions and the vertical position within the canopy. On sunny days, the rate of net photosynthesis typically increased in the morning, followed by a decrease in the afternoon, characterized by a midday depression around 13:00 h, with two peak values observed at 12:00 and 14:00 h. This diurnal pattern aligns with the findings of Leverenz [31]. Conversely, on cloudy days, no midday depression was observed. Interestingly, leaves in the lower canopy also did not display a midday depression. The diurnal variation in photosynthesis can be influenced by various environmental and physiological/biochemical factors [43]. For instance, this study found that photosynthesis rates were generally positively correlated with PAR, while an inverse relationship was observed with ambient CO₂ concentration (Figure 6). However, the remarkably consistent diurnal pattern of photosynthesis observed throughout the growing season suggests that the regulation of photosynthesis in Camphor tree forests follows a robust internal rhythm [44]. Moreover, the fact that the midday depression of photosynthesis occurred exclusively on sunny days but not on cloudy days implies that this depression results from intricate interactions between internal regulatory mechanisms of photosynthesis and external environmental conditions, particularly PAR. These interactions, along with the underlying physiological and biochemical mechanisms governing the internal rhythm of photosynthesis in this species, warrant further investigation [45].

We observed that the rates of photosynthesis declined along the vertical canopy profile in the studied forests. The daily average of photosynthetic rates in the middle and lower canopies accounted for approximately 83% and 25% of that observed in the upper canopy, respectively. Our results were consistent with the findings from other studies. It was found that the light-saturated photosynthetic rate declined by 27% and 36% in Douglas fir and western hemlock, respectively, between the upper canopy and the lower canopy [46]. Leaf photosynthesis decreased from the top of the canopy downwards, showing a significant vertical gradient in a poplar plantation [47]. The observation that the magnitude of diurnal fluctuations in photosynthesis in camphor trees was smaller on cloudy days than on sunny days, as well as smaller in the lower canopy compared to higher canopy positions, raises interesting considerations. The reduced fluctuations in photosynthesis on cloudy days may be linked to the relatively stable levels of PAR experienced on overcast days. Studies have indicated that PAR levels within the forest canopy are more consistent on cloudy days compared to sunny days [48,49]. Additionally, other environmental factors, such as temperature, often vary with light levels and are also presumed to be more stable on cloudy days. These combined factors could contribute to the smaller fluctuations in photosynthesis on cloudy days in comparison to sunny days [50]. However, the smaller fluctuations in photosynthesis observed in leaves in the lower canopy, as opposed to what might be expected, raise intriguing questions. Despite the study site’s relatively low latitude (27°50′ N), resulting in a smaller sun angle, one might anticipate that the PAR level beneath the forest canopy would exhibit more variability at the lower canopy positions [51]. This expectation stems from the notion that the shading effect of the forest canopy should be more pronounced in the early morning and late afternoon. Consequently, one might expect the rate of photosynthesis in lower canopy leaves to exhibit greater fluctuations rather than smaller ones when compared to higher canopy positions [52]. The study suggests that the smaller fluctuations in photosynthesis in the lower canopy could reflect the acclimation of these leaves to lower light conditions. Data from the study indeed demonstrate that lower canopy leaves exhibit an acclimation to reduced light conditions. For instance, when compared to leaves at higher canopy positions, lower canopy leaves displayed a lower light compensation point, a lower light-saturated rate of photosynthesis, a lower respiration rate, and a lower initial slope in response to changes in CO₂ concentration, but they exhibited a greater apparent quantum yield (Figure 3 and Figure 4). It is also possible that morphological adaptations occurred. These acclimations allow lower canopy leaves to efficiently utilize low PAR levels, particularly during the early morning and late afternoon, but may render them less efficient in harnessing higher PAR levels, which occur during late morning to early afternoon [51,53]. This contrasts with leaves in higher canopy positions, which appear to exhibit the opposite response. Consequently, lower canopy leaves exhibit smaller diurnal fluctuations in photosynthesis compared to those at higher canopy positions.

The data collected in this study revealed that camphor trees have strategically optimized their allocation of nitrogen resources within the photosynthetic apparatus across different vertical layers of the canopy. This adaptation allows them to efficiently harness varying light conditions at different canopy positions. Leaves in the lower canopy exhibit a remarkable ability to utilize limited light resources, with an apparent quantum yield of photosynthesis nearly twice as high as their counterparts in the upper canopy [54]. These lower canopy leaves also display reduced dark respiration rates, conserving carbon during periods of low light availability. Moreover, their lower light compensation point indicates efficient photosynthesis initiation under reduced light levels. Conversely, upper canopy leaves are adept at maximizing photosynthetic productivity in high-light conditions. They allocate more resources to capture and assimilate carbon efficiently [55]. These findings underscore the importance of an optimized nitrogen allocation strategy in camphor trees, enhancing their adaptation to varying light conditions throughout the canopy layers, and aligning with the concept of functional convergence observed in other tree species [49]. Overall, the mean values for stand biomass (144.7 t ha⁻¹) and biomass carbon storage (71.6 t C ha⁻¹) in the surveyed Camphor tree forests were consistent with previous research findings. Notably, Wang et al. [48] reported an average individual tree carbon storage of 0.05 t tree⁻¹ in the Taiwan region, equivalent to approximately 80 t C ha⁻¹ at a stand density of 1600 trees per hectare. Additionally, Lei et al. [49] observed a carbon storage of 45.1 t C ha⁻¹ in the overstory tree layer of 18-year-old Camphor tree forests in tropical regions. The photosynthesis patterns in camphor trees displayed a seasonal variation characterized by two peaks in June and September, with the June peak being more pronounced. Notably, there was a significant “mid-summer depression” in photosynthesis during July and August. This seasonal pattern bears similarity to observations made in a nine-year-old loblolly pine forest [50]. However, it contrasts with findings from black spruce seedlings in a semi-natural environment, where the rate of photosynthesis steadily declined throughout the growing season [56]. This seasonal pattern likely results from complex interactions between leaf physiology and environmental conditions. From March to June, the region experiences increasingly favorable environmental conditions for tree physiology and growth, leading to a steady rise in physiological activity and growth. However, this active growth phase may rapidly deplete soil moisture and other essential resources. Moreover, July and August represent the hottest months with the highest solar radiation levels in the region, creating stressful conditions that could reduce the photosynthetic activity and the effectiveness of certain protective mechanisms, further depressing photosynthesis [57]. Notably, the “mid-summer depression” in photosynthesis observed by Murthy et al. (1997) coincides with the peak air temperatures in the season [50]. The second peak of photosynthesis in September is likely attributed to increased rainfall and cooler temperatures. However, as October and November approach, trees in the region typically initiate cold-hardening processes and bud setting. With these processes occurring alongside less favorable environmental conditions, it is expected that the rate of photosynthesis would decline during these months.

It is important to exercise caution when extrapolating the findings of this study to natural forests. This research was conducted in a plantation forest, which exhibits structural differences when compared to natural forests. These distinctions include lower stem density and reduced crown closure in plantations relative to natural forests, as well as a more uniform size and genetic composition in plantations [58]. While the specific variances in the seasonal and vertical patterns of physiological traits between plantations and natural forests of the same species remain poorly understood, it is reasonable to suspect significant differences. For instance, in natural forests, there is typically a gradual decline in photosynthetic capacity from the upper to the lower canopy [49]. In contrast, the disparity in photosynthesis between the upper and middle canopy layers was relatively minor compared to the abrupt reduction observed from the middle to the lower canopy in the camphor tree plantation of this study (Figure 2c and Figure 5). This dramatic drop in photosynthesis in the lower canopy may be attributed to the shading effect of understory vegetation growing beneath the relatively open canopy of the plantation. Such disparities should be thoroughly investigated and carefully considered when applying the study’s results, particularly in cases where findings at the leaf level are extrapolated to the canopy or broader landscape.