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Official Journal of the Japan Wood Research Society

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Phenological activities of cambium and inter-annual variations of Pinus densiflora saplings upon CO2 enrichment

Journal of Wood Science volume 71, Article number: 57 (2025) Cite this article

Abstract

The current study investigated the long-term effects of CO2 enrichment on cambial activity and wood tracheid traits of Pinus densiflora grown in Open Top Chambers (OTCs). We monitored the cambial activity and analyzed quantitative and qualitative variations in the tracheid at different CO2 enrichments. The cambial activity in the trees was found to begin in mid-to-late March and end in late October to early November. So, the growing season was a little longer than the monitoring period. The time of maximum growth rate was delayed as CO2 enrichment increased, thereby suggesting that rising CO2 concentration may affect intra-annual cambial activity. The quantitative growth (number of cells) increased with higher concentrations of CO2 in the early years of the CO2 exposure. However, a decline in growth was observed from the 8th year after exposure. Qualitatively, cell wall thickness was found to be the largest for the highest CO2 treatment, which was in contrast to previously reported pot experimental results obtained over a couple of growing seasons. The observed quantitative growth increase coupled with the qualitative variations (increased cell wall thickness) may influence the physical properties of wood and carbon storage capacity, and such knowledge is important for forest resource utilization and management planning.

Introduction

Global warming and related climatic changes are currently the major threats to our planet. In this regard, the increase in atmospheric CO2 due to heavy use of fossil fuel and indiscriminate development of urban systems which destroy the ecosystem has been identified as the primary causes of this climate change. As of 2024, the level of atmospheric CO2 has reached ≈ 420 ppm, which is about 50% higher than the pre-industrial level, and this level has been reported to be increasing continuously [1]. Such increase in the CO2 concentration in the atmosphere affects plant physiology and growth directly, imparting certain effects cumulatively over long periods [2,3,4]. Many countries have already focused on carbon neutrality where forests and wood play crucial roles in CO2 absorption and storage [5,6,7]. In this regard, quantitative and qualitative variations in trees can be used to assess CO2 absorption and storage capacity. On the other hand, most of the carbon emission factors primarily use external variables, such as diameter at breast height and tree height [8,9,10,11,12].

Environmental variations have been reported to affect cambial activity, the meristematic tissue responsible for tree growth [13]. Understanding this cambial activity enables one to comprehend tree growth better. For example, the onset and cessation of cambial activity allow one to estimate the accurate duration of radial growth, while the trend of cambial activity provides insights into the seasonal characteristics of the radial growth [14,15,16,17]. Now, the xylem cells produced due to cambial activity store various information about environmental factors that affect tree growth during the growing season [18, 19]. Thus, the xylem cell traits, such as cell diameter, lumen diameter, and cell wall thickness, serve as the evidence to validate the effects of climate and environmental variations on tree growth [20,21,22]. CO2 is one of the primary substrates in photosynthesis, and the carbohydrates produced via photosynthesis are the main components of the cell walls [23]. Therefore, wood tracheid traits have been examined to understand tree responses to variations in CO2 enrichment [24].

Research on the effects of CO2 enrichment on plants has been actively going on for the last two decades [23, 25,26,27,28,29,30,31]. Unlike the other studies of environmental factors causing climate change, the CO2-related plant research requires special facilities that can maintain a constant CO2 concentration [29, 32]. To this end, various types of CO2 treatment facilities have been developed, among which the open-top chambers (OTCs) and free air CO2 enrichment (FACE) systems are the significant ones [32,33,34,35,36]. The FACE systems are ideal for long-term studies under natural environmental conditions, but they incur high maintenance costs [28, 37]. By contrast, the OTCs are less expensive, suitable for medium to long-term studies, and are thus widely used [25, 29].

The response of woody plants, mainly the trees, to increased CO2 enrichment is complex. This is because tree growth is influenced by various environmental factors besides CO2. Some previous studies have shown that the effect of CO2 enrichment on tree growth is smaller than expected, or even non-existent [38]. Nevertheless, most plants have shown increased photosynthetic rates and enhanced growth when atmospheric CO2 enrichment occurs [39, 40].

The current study investigated the long-term effects of CO2 enrichment on cambial activity and wood tracheid traits of Pinus densiflora grown within Open Top Chambers (OTCs). The specific objectives of the current study are—(1) examine the differences in the intra-annual xylogenesis of P. densiflora under different CO2 enrichments, and (2) analyze variations in tracheid both quantitatively and qualitatively over a 10-year study period (2012–2021). The results are expected to provide valuable insights for predicting the growth response of P. densiflora in future climate change scenarios and help establish important baseline data to predict certain variations in forest ecosystems.

Materials and methods

Study site

The study was done in 3 Open Top Chambers (OTC I, II, III) which were located in the Forest Bioresources Department of National Institute of Forest Science, Suwon, and completed in August 2009. The OTCs had a decagonal structure with a diameter of 10 m, height of 7 m and a 45° aligned roof designed to maintain an upper opening ratio greater than 75% [41]. The site comprises three treatment areas.

The CO2 enrichments inside the OTCs were different, as shown below and in Fig. 1:

  • OTC I: ≈ 400 ppm, equivalent to atmospheric CO2 enrichment

  • OTC II: ≈ 560 ppm, 1.4 times the atmospheric CO2 enrichment

  • OTC III: ≈ 720 ppm, 1.8 times the atmospheric CO2 enrichment

Fig. 1

An open top chamber (OTC) at Suwon, the Republic of Korea

In September 2009, six representative tree species from Korea’s central temperate region were planted inside each OTC, comprising three individual trees from each species. These 6 species were Korean red pine (P. densiflora), sawtooth oak (Quercus acutissima), east Asian ash (Fraxinus rhynchophylla), Korean maple (Acer pseudosieboldianum), mountain hawthorn (Crataegus pinnatifida), and Korean mountain ash (Sorbus alnifolia). In this study, P. densiflora was investigated, and only the 4-year-old seedlings grown from the same clone were selected for planting in the OTCs [42]. The CO2 exposure was started in April 2010 and was employed from 8 AM to 6 PM every day throughout April to November each year [41].

Cambial activity

Micro-cores were collected from three P. densiflora trees from each OTC during the period late March to October 2019. A mini-increment borer (Trephor) having 2 mm diameter was used, and two samples were obtained from each tree in each collection. The collected microcores were embedded in PEG2000, and 6–12 μm thick sections were prepared using a sliding microtome. The sections were then double-stained with a mixture of 1% Safranin and 0.5% Astra Blue, and subsequently mounted in 50% glycerin. The cambial activity was observed under an optical microscope. The first appearance of the enlarged cells in the cambial zone was considered as the onset of the cambial activity (Fig. 2b). The cessation of the cambial activity was marked at the point where (1) no further cell division occurred in the cambial zone, and (2) the number, shape, and size of the dividing cells became stable, i.e. showed no further change and resembled a dormant cambial zone (Fig. 2c). To investigate the growth pattern of the diameter, the widths of the newly formed xylem cells were measured at 4-week intervals. The radial increment was measured from the previous year’s annual ring boundary up to where the enlarged cells were located (Fig. 2).

Fig. 2

Transverse sections at different cambial activity (A): dormant season (before beginning of cambial activity), B the beginning of growing season, C the cessation of cell division in the cambial zone, D the cessation of lignification, and E measurement method of radial increment (Ca: cambium, Xy: xylem, EC: enlarging cell, Ph: phloem) (— Scale bars A, B, C, D = 50 μm, E = 100 μm)

In the statistical analysis of the cambial activity, Gompertz equation [43, 44] was applied to examine the growth trends of P. densiflora in each OTC. The Gompertz equation was differentiated to determine the day of the year (DOY) of the maximum growth rate [44].

Analysis of tracheid traits

In 2022, the OTC facilities were dismantled, and nine P. densiflora disks were collected from each treatment group (three disks from each OTC). The average diameter of the disks was determined from the disk’s long and short diameters. The ring widths were measured in 3 or 4 directions and cross-dated [42]. To eliminate any eccentric growth effect, the compression and opposite wood were avoided while determining the representative direction for measuring tree-ring parameters. To obtain transverse thin sections from the disks, 10 mm wide wood strips including the pith were first cut from the disks. Next, the 10 mm wide wood strip was divided into two 5 mm wide wood sticks—one for cutting thin sections from even years and the other for cutting from odd years. The 12–15 μm-thick transverse section was then cut using a sliding microtome and imaged using a slide scanner (Axio Scan Z1, ZEISS). Cell analysis was done with respect to the last 10 years (2012–2021) using WinCELL program (Regent, Canada). From each annual ring, more than 5 radial files were selected to measure the cell diameter (CD), lumen diameter (LD), and cell wall thickness (CWT).

To compare the anatomical characteristics between the OTCs, R software was used with outlier-removed data (Table 1). The detection of the outliers was based on Tukey’s method using boxplot statistics, where the values falling beyond 1.5 times the interquartile range (IQR) were considered outliers [45]. Furthermore, to reduce the inflation of F-values caused by large sample sizes, 500 observations were randomly selected from each treatment group using the ‘sample_n()’ function in R. This stratified subsampling ensured a statistical balance across the 3 OTCs. Also, one-way ANOVA was applied, followed by Duncan’s multiple range test to assess the significant differences between the treatments.

Table 1 The number of cells used in analysis (ALL: all cells measured in WinCELL, CLEAN: the number of cells with outliers removed in R, CD: cell diameter, LD: lumen diameter, CWT: cell wall thickness)

Results

Cambial activity

To observe the cambial activity in P. densiflora from each treatment group, sample collection was started on March 22, 2019. A close examination of the samples revealed that cell division had already started in the cambial zone of all the trees. In the samples, 1–2 cells were found in the cell division or enlargement phase, thereby suggesting that the cambial activity had already begun a few days back or a week earlier. On the final sampling day, October 24, 4 out of 9 trees ceased cell division in the cambium: one in OTC I, two in OTC II, and one in OTC III. Although the remaining trees (two in OTC I, one in OTC II, and two in OTC III) still underwent cell division, observations suggested that their cell division would also terminate within a week or so. Accordingly, no significant difference in cambial activities was observed among the OTCs.

All P. densiflora in the OTCs showed S-shaped growth curves, but the curve for the OTC II treatment was the least distinct (Fig. 3). The maximum growth rate was first observed in the OTC I treatment, followed by OTC II and OTC III. There is a clear difference in the timing of the maximum growth rates for OTC I in mid-May (DOY 135), OTC II in early June (DOY 157), and OTC III in late June (DOY 180) (Fig. 4).

Fig. 3

Monthly variations of radial increment in 2019 (black line: mean curve) for all the open-top chambers (DOY: day of the year)

Fig. 4

The accumulated and daily growth in 2019 (the vertical line is the duration of the maximum radial growth rate, DOY: day of the year)

Quantitative variations in the tracheids

A comparison of the common measures of tree volume growth, namely the stem diameter, ring width, and number of tracheids, collected from the disks showed that the stem diameter and tracheid number increased with increasing CO2 enrichment in the OTCs (Table 2).

Table 2 Quantitative growth variation (stem diameter, ring width, and the number of cells) in each open top chamber

A time series comparison of the number of cells over the past 10 years showed a similar trend for all the 3 OTCs. All the OTCs first displayed an increase in the number of cells till 2017, which then decreased. To note, OTC II and OTC III showed more distinct changes than OTC I (Fig. 5).

Fig. 5

The annual quantitative (number of cells) variation for 10 years in the three open top chambers (three trees in each OTC, with at least five radial files measured in each tree for each year)

Qualitative variations in the tracheids

To determine the qualitative changes in the tracheids, each tracheid trait (CD, LD, CWT) in the time series was compared. It was found that the CD and LD remained constant over the entire 10-year period in all the OTCs (Fig. 6). The CWT also remained relatively constant, with a slight decrease in the last year, i.e. 2021, though this change was statistically significant. Therefore, in general, the tracheid traits remained constant and did not change significantly with increase in the CO2 concentration and exposure period.

Fig. 6

The annual qualitative (cell traits) variation for 10 years for all the open top chambers (LD: lumen diameter, CD: cell diameter, CWT: cell wall thickness, see Table 1 for the number of each value)

Comparing the median values of the measurements (Table 3), the CD and LD lengths were in the order OTC I > OTC III > OTC II (p < 0.05), and the CWT was in the order OTC III > OTC II = OTC I (p < 0.05). These results indicated that the effect of CO2 on the cell traits was relatively more pronounced in CWT than in the CD or LD. According to the ANOVA and Duncan test results (Table 4), all measured anatomical parameters showed statistically significant differences between the OTCs (p < 0.001). Based on CD and LD, OTC I and OTC III were classified into the same group ‘a’, while OTC II was assigned to a separate group ‘b’. On the other hand, with respect to CWT, OTC I and OTC II were placed into the same group ‘b’, while OTC III was classified into a different group ‘a’.

Table 3 Qualitative growth variation (cell diameter, lumen diameter, cell wall thickness) in each open top chamber
Table 4 Results of ANOVA and Duncan test using qualitative growth variation (cell diameter, lumen diameter, cell wall thickness) (***: p < 0.001)

Discussion

The monitoring of cambial activity allowed accurate determination of the diameter growth period in the sampled trees. In the past studies concerning Open Top Chamber (OTC) system, the CO2 exposure was applied from April to November each year and the growing period was set from May to October. Moreover, the previous studies on cambial activity in the Republic of Korea were usually conducted after April, and in some cases, the studies even began in May depending upon the altitude and species [17, 46,47,48]. Meanwhile, the present study found that the cambial activity actually started in all the trees even before March 22, the current sample collection date. This observation was identical to that of Kwon and Kim [49] who investigated P. densiflora and P. koraiensis in the lowland of Chuncheon in 2002 [49]. Furthermore, most previous studies monitoring the cambium activity focused on the limited response to temperature [50,51,52,53,54,55], and they reported that the temperature plays a crucial role in initiating cambial activity in trees. Considering that the OTCs showed an average temperature difference of 0.74 °C and a maximum of 1.44 °C compared to the control [41], future studies will consider the time of onset of the cambial activity under similar facilities and operation plans. A recent report stated that temperature determines the timing of growth and nutrient availability determines the rate of growth (Kuželová et al., under review). Since the nutrients modulate the tree growth rates, the trees on the north slopes with higher nutrient content displayed higher absolute growth rates. By contrast, the present study confirms that maximum growth rate occurs as CO2 concentration increases. Since the OTCs were identical in terms of other conditions (soil conditions, surrounding vegetation), our study suggests that atmospheric CO2 concentration, in addition to the nutrients in the soil, is another important factor in determining tree growth rate and the timing of the maximum growth. Furthermore, the results support the theory [56] that the synthesis of carbohydrates through photosynthesis influences the formation of the meristems.

To examine the quantitative variations in the tracheid of P. densiflora with respect to CO2 enrichment, the stem diameter, annual ring width, and number of tracheids were compared, and the stem diameter displayed the most distinct difference. Time series analysis of the quantitative variations in tracheid indicated that the CO2 enriched OTCs showed an increasing trend until 2016, followed by a decreasing pattern from 2017. This confirmed that the growth of the tracheids does not continuously increase with increasing CO2 concentration, but reduces after a certain period. This result can be interpreted in terms of three main factors, based on prior research and empirical field observations. The first factor is the effect of CO2 fertilization. Most of the prior studies reported an increased plant growth even if the photosynthetic capacity was reduced due to high CO2 concentration [32, 34, 57, 58]. Unlike the present study, which is based on 10-year monitoring data, those studies used data collected over relatively shorter periods, typically a few years [31]. As a result, the past studies might not have captured the point at which growth decline occurred due to reduction in photosynthetic capacity by CO2 enrichment. The second factor involves changes in primary metabolism due to decline in leaf nitrogen. Nitrogen plays an important role in determining the maximum carboxylation rate, as it is the key component of photosynthetic enzymes [59, 60]. However, prolonged exposure to high concentration of CO2 can lead to decrease in the available nutrients in the soil. As nutrient consumption surpasses the nutrient supply, the photosynthetic capacity of plants may decline. A decrease in the concentration of nitrogen absorbed by the plants leads to lower nitrogen levels in the leaves, thereby reducing photosynthesis, which is closely linked to tree growth [61]. The last factor is the shading effect caused by crown growth. When the trees were initially planted, the spacing between them was sufficient to avoid crown overlap; however, by the year of harvesting, the trees grow and their enlarged crowns start to overlap (Fig. 1). The shading effect resulting from crown overlap likely induces the previously mentioned photosynthesis reduction, thereby influencing the diameter growth of the experimental trees. In the current study, these effects appeared to be evident from the seventh year after the start of CO2 exposure in all the OTCs, including OTC I. Although the current study did not monitor the annual development of the crown, thereby limiting the quantitative assessment of the shading effect on tree growth, it is imperative that future research in this area consider such effect to obtain a more comprehensive understanding.

In regard to qualitative growth variations, no consistent effects of CO2 enrichment on cell diameter and lumen diameter were found in the current study. However, the cell wall thickness was found to be affected, being the thickest in OTC III, which had the highest CO2 enrichment (Table 3). Some previous studies on larch and P. densiflora reported that with an increase in CO2 enrichment, the lumen diameter also increased while the cell wall thickness decreased [24, 62]. However, other studies on the same coniferous species have shown that the cell wall thickness increases with elevated CO2 concentrations [63,64,65,66]. These results indicate that the CO2 concentration does not have the same effect on the anatomical characteristics of trees, and this may be due to the differences in the species, age, environmental conditions, and other complex factors [31, 67]. Pot experiments have been criticized for their inability to exclude the inhibitory effects of container constraints on root growth and nutrient uptake [23]. Similarly, chamber experiments face limitations due to edge effects, making it difficult to realistically simulate a natural and managed ecosystem [23]. These considerations underscore the importance of detailed experimental design while studying plant responses to changes in CO2 concentration.

Conclusions

The current study examined the changes in cambial activity and wood cell characteristics of P. densiflora with respect to elevated CO2 concentrations. The findings indicate that an increased CO2 concentration resulted in delayed maximum growth rates and increased cell wall thickness. Furthermore, the number of cells showed a declining trend rather than a continuous increase throughout the CO2 treatment period. These results suggest that the impact of elevated CO2 concentration on pine growth is not simple and stimulatory but exhibits complex patterns over a long-term period. Notably, the qualitative changes (increased cell wall thickness) and quantitative growth enhancement can influence the physical properties of wood and carbon storage capacity of trees, thereby carrying significant implications for future forest resource utilization and management planning.

The present study offers a promising data baseline for predicting the future of Korean forests and developing management strategies in response to climate change. However, since the study was conducted on young trees, further research on the responses of mature trees based on long-term observations is necessary. Additional physiological investigations, such as photosynthetic rate and water use efficiency, would enable a more comprehensive interpretation. Lastly, extending similar studies to other major tree species in Korea would allow for more accurate predictions of the overall responses of the Korean forest ecosystem to climate change.

Availability of data and materials

The data sets analyzed during the present study are available from the corresponding author upon reasonable request.

Abbreviations

OTC:

Open top chamber

FACE:

Free air CO2 enrichment system

DOY:

Day of a year

CD:

Cell diameter

LD:

Lumen diameter

CWT:

Cell wall thickness

IQR:

Interquartile range

ANOVA:

Analysis of variance

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Acknowledgements

National Institute of Forest Science of the Republic of Korea, Grant No. FG0401-2025年01月20日25.

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Authors and Affiliations

  1. Tree-Ring Research Center, Chungbuk National University, Cheongju, 28644, Republic of Korea

    Jun-Hui Park & Jeong-Wook Seo

  2. Chronological Research, Institute for Space-Earth Environmental Research, Nagoya, 464-8601, Japan

    En-Bi Choi

  3. Department of Forest Bioresources, National Institute of Forest Science, Suwon, 16631, Republic of Korea

    Hyemin Lim

  4. Department of Wood and Paper Science, Chungbuk National University, Cheongju, 28644, Republic of Korea

    Jeong-Wook Seo

Authors
  1. Jun-Hui Park
  2. En-Bi Choi
  3. Hyemin Lim
  4. Jeong-Wook Seo

Contributions

JHP and JWS designed the research layout. JHP, EBC, and HL conducted field experiments. JHP and EBC collected and analyzed the data in the laboratory. JHP performed the statistical analysis and draft the manuscript. JWS revised the manuscript. All authors discussed the results and conclusions, and contributed to writing the final version of the manuscript.

Corresponding author

Correspondence to Jeong-Wook Seo.

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Park, JH., Choi, EB., Lim, H. et al. Phenological activities of cambium and inter-annual variations of Pinus densiflora saplings upon CO2 enrichment. J Wood Sci 71, 57 (2025). https://doi.org/10.1186/s10086-025-02229-6

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  • DOI: https://doi.org/10.1186/s10086-025-02229-6

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