1. Introduction

Warming-induced shifts in plant phenology has been widely reported in recent decades, with potentially significant impacts on the composition and functioning of forest ecosystems (Forrest and Miller-Rushing, 2010; Piao et al., 2019; Fu et al., 2020). Increasing evidence showed that an advancement in spring leaf unfolding and a delay in autumn leaf senescence, resulting in an extended growing season that could enhance forest productivity (Fu et al., 2018; Chen et al., 2019; Gao et al., 2022). Additionally, research efforts have explored how different phenological phases and the intervals between them respond to warming, such as the unequal shifts in flowering and fruiting, as well as the time intervals among leaf unfolding, flowering, and fruiting under warming conditions (Ma et al., 2021, 2022; Li et al., 2024). While the phenology of primary growth in trees is relatively well understood, the phenological responses of secondary growth processes, particularly cambial activity and xylem development, to climate warming remain poorly studied. Importantly, most existing research on xylem phenology has concentrated on conifer species in boreal or alpine regions (e.g., Cuny et al., 2015; Rossi et al., 2016; Huang et al., 2023), largely due to the regular structure and accessibility of their wood tissues. In contrast, broadleaf species, which dominate many temperate and mixed forests, have received far less attention in xylem phenological studies. This creates a substantial knowledge gap, especially given their ecological and functional significance in forest carbon cycling and biodiversity. Expanding xylem phenology research to broadleaved trees is thus essential for a more comprehensive understanding of forest responses to climate warming across different forest types.

Xylem cell enlargement and wall-thickening are two critical phenological events of secondary growth, signifying the onset of stem growth and woody biomass production, respectively (Cuny et al., 2015). Warming-induced shifts in the timing of these events can significantly influence forest ecosystem dynamics and their carbon storage capacity. Changes in xylem cell enlargement timing have direct consequences on tree growth, potentially affecting biomass accumulation rates and overall forest productivity (McDowell et al., 2008). For instance, earlier cell enlargement in response to warmer temperatures may lead to an extended growing season, but if it occurs too early, it could increase the risk of spring frost (Rossi et al., 2011). Changes in wall-thickening timing, which plays a crucial role in the formation of woody tissue, could also have long-term implications for tree structure and stability. Alterations in this process may influence how trees respond to environmental stresses, such as droughts or extreme temperatures, potentially reducing forest resilience (Anderegg et al., 2020). Moreover, these shifts in secondary growth phenology can indirectly affect forest ecosystem functioning by altering tree competition, species composition, and overall forest community dynamics. For example, species with faster or more resilient secondary growth may become dominant under warmer conditions, potentially displacing slower-growing or more sensitive species and leading to shifts in community structure (Pugnaire et al., 2011).

Temperature is the primary candidate for environmental factors driving the initiation of xylem cell enlargement and wall-thickening in temperate trees (Rossi et al., 2016; Cuny et al., 2019; Huang et al., 2023). Trees often require a certain exposure to chilling temperatures during winter to release endodormancy before xylem development can proceed (Begum et al., 2018; Huang et al., 2020). This chilling phase ensures that the transition from dormancy to activity is synchronized with favorable environmental conditions, reducing the risk of frost damage to newly formed xylem cells (Begum et al., 2013; Delpierre et al., 2016; Hanninen, 2016). Once chilling requirements are fulfilled, the accumulation of forcing temperatures (defined as the sum of temperatures above a specific threshold) triggers cambial resumption and subsequent xylem formation (Antonucci et al., 2015; Delpierre et al., 2019). However, warm-induced reductions in chilling accumulation may lead to an increased requirement for forcing temperatures, potentially delaying the initiation of secondary growth (Ford et al., 2016; Delpierre et al., 2019). This interaction between chilling and forcing creates a nonlinear relationship between temperature changes and the timing of xylem phenology, complicating predictions of tree growth responses under future climate scenarios (Fu et al., 2015; Rossi et al., 2016). In addition, photoperiod serves as another critical factor influencing the onset of cell enlargement and wall-thickening in various tree species (Way and Montgomery, 2015; Huang et al., 2023). Experiments conducted in controlled environments have demonstrated that extended daylength can significantly accelerate spring phenology (Caffarra and Donnelly, 2011). Moreover, water availability plays a crucial role in the spring resumption of plants, particularly in regions with winter water deficits (Ren et al., 2015; Li et al., 2021). Low winter temperatures can lead to dehydration stress, requiring the restoration of water balance before the onset of spring growth, as adequate turgor pressure is vital for tree growth (Ben-Gal et al., 2010).

Phenological events are unlikely to respond to climate warming independently. The shifts in early-season events may influence the timing and responses of subsequent events (Ettinger et al., 2018; Ma et al., 2021). The timing of cell wall-thickening depends on both enlarging time and the interval between them. The variation of the time interval is closely related to the required forcing and temperature during this period. Assuming a fixed amount of forcing is required for the development of enlarging cells, rising temperatures accelerate the accumulation of forcing, thereby shortening the interval between cell enlargement and wall-thickening. However, if warming alters the balance of carbon allocation, such as prioritizing primary growth or reproduction, the required resources for wall-thickening may become limited, potentially prolonging the interval. Additionally, other environmental factors, such as water availability and photoperiod, may modulate the response of this interval to warming. For instance, increased water availability during early growth stages might enhance turgor-driven cell expansion, leading to a more rapid transition to wall-thickening (Li et al., 2021). Conversely, photoperiod, which influences the seasonal progression of cambial activity, may constrain how much warming can shorten or lengthen this interval (Huang et al., 2023). Given these complex interactions, we hypothesize that climate warming will lead to unequal changes in the timing of cell enlargement and wall-thickening, altering the duration of the interval between these events.

Using xylogenesis observation data from twelve common tree species in mixed broadleaved Korean pine (Pinus koraiensis) forests of Northeast China collected between 2019 and 2024, we aimed to (1) analyze and quantify the temporal change of the onset of xylem cell enlargement, wall-thickening, and the interval between these stages, and (2) investigate their responses to climate warming. To address the second objective, we assessed the influences of chilling, forcing, precipitation, and photoperiod on these phenological events and their associated time intervals.

2. Material and methods 2.1. Study region and species

The study was conducted in the Changbai Mountain National Nature Reserve, which features a typical temperate continental montane climate, characterized by warm, rainy summers and long, cold winters. The mean annual precipitation is 682.3 mm, and the mean annual temperature is 3.6 ℃. July, the warmest month, has an average temperature of 19.7 ℃, while January, the coldest month, averages −15.6 ℃. The broad-leaved Korean pine forest and the poplar–birch forest represent two dominant forest communities in the region. To capture species-level phenological responses representative of these communities, we selected twelve dominant and co-dominant tree species based long-term forest inventories and previous ecological surveys (Xu et al., 2024). Detailed information on these species is presented in Table 1, and their xylem anatomical characteristics are depicted in Fig. 1.

2.2. Environmental data collection

Environmental data used in this study included air temperature, precipitation, and photoperiod. Air temperature was measured at the sampling plots using HOBO sensors (Pro v.2, Onset Computer Corporation, USA) installed at a height of 1.5 m above the ground, with data recorded hourly. Daily precipitation data were sourced from a nearby meteorological station located less than 2 km away. Photoperiod (daylength) was calculated using the R package “insol” based on the geographic coordinates and dates of observation. Although photoperiod is consistent for a given calendar date and location across years, it differed among individual trees because the timing of cell enlargement and wall-thickening onset varied. Therefore, each tree experienced slightly different daylengths at the onset of these growth phases.

Chilling requirements are typically defined by the duration which temperatures remain within a specific range. To assess the effect of chilling on spring phenological events, we calculated the number of days with daily average temperatures between 0 ℃ and 5 ℃ based on the period from November 1st of the previous year to the onset date of cell enlargement and wall-thickening. Forcing temperature was determined as the cumulative sum of temperatures exceeding 5 ℃ from January 1 to the respective onset dates. Total precipitation was calculated over the same period, from January 1 to the onset date of cell enlargement and wall-thickening.

2.3. Sample collection and experiment

Xylogenesis was monitored weekly from 2020 to 2024 and every ten days in 2019 using an increment borer (2019) or a Trephor (2020–2024). Sampling was carried out from mid-April to mid-October each year, ensuring full coverage of the growing season for all species. Data on the onset of cell enlargement and wall-thickening were not collected in 2022. For each species, from 4 to 9 adult dominant trees with upright, healthy, and unbiased crown trunks were selected every year. Tree cores were extracted from the trunk at breast height (1.3 ± 0.3 m) along a spiraling trajectory, with each sampling spaced at least 3 cm apart to minimize wounding interference. The cores were stored immediately at 4 ℃ in FAA solution (70% ethanol: formalin: acetic acid = 9: 0.5: 0.5) to avoid tissue deterioration. In laboratory, the cores were oriented by marking the transverse side for accurate sectioning. They were softened in glycerol and tert-butanol (50%, 70%, 85%, 95%, and 100%) and dehydrated in a graded ethanol series. Samples were then embedded in paraffin, and 10–12 μm thick cross-sections were cut using a rotary microtome (RM2235, Leica, Germany). Sections were stained with safranin and fast green to enhance cellular contrast and observed with bright-flied and polarized light to differentiate the developing xylem cells.

The classification of xylem cells at different developmental stages follows a standardized protocol across all tree species. For each section, the width of cells in the enlargement and wall-thickening phases were counted along three radial rows. Enlarging cells typically feature thinner walls compared to cambial cells and possess a significantly larger radial diameter (Rossi et al., 2007). Wall-thickening cells were distinguished from enlarging cells by the birefringence of their secondary cell walls under polarized light. Mature cells had completely lignified cell walls without protoplasts, and were stained purplish red by safranin. For each tree, the onset of cell enlargement and wall-thickening in a given year was determined as the date when the first enlarging or wall-thickening cell was observed. The precise timing of these developmental stages was estimated using linear interpolation (Michelot et al., 2012). These dates were recorded as the day of the year (DOY) and designated as the cell enlargement DOY and wall-thickening DOY, respectively.

2.4. Statistical analysis

We used the onset dates of cell enlargement and wall-thickening, as well as the time intervals between these two events, as response variables. Linear mixed-effects models were employed to assess the influence of chilling, forcing, photoperiod, and precipitation, with tree species included as a random effect to account for species-specific variation. To explore the association between the timing of the two phenological events, linear regressions were conducted between cell enlargement DOY and wall-thickening DOY. One-way ANOVA was performed to evaluate both intra- and interspecific differences in the timing of these events. To capture potential nonlinear trends, we further applied data-driven and flexible generalized additive models (GAMs) (Lai et al., 2024) to examine how the relative time interval between cell enlargement and wall-thickening varied in response to environmental drivers. Additionally, we tested interactions between the environmental variables and found that their contributions to the variation in the response variables was minimal. Therefore, interactions were not included in the final model. The relative importance of each predictor was evaluated using the R package “glmm.hp” (Lai et al., 2022, 2023).

3. Results 3.1. Temporal changes of cell enlargement, wall-thickening and the time interval

The onset timing of cell enlargement and wall-thickening varied significnatly among species (P < 0.05). Specifically, cell enlargement DOY ranged from DOY 115 in Phellodendron amurense to DOY 167 in Tilia amurensis, while wall-thickening DOY ranged from DOY 123 (Ulmus japonica) to DOY 160 (T. amurensis) (Table 2). By comparing the slopes of the two phenological events across species, we found that the slope for the onset of wall-thickening was consistently steeper than that for cell enlargement, indicating that the timing of wall-thickening advanced more rapidly than that of cell enlargement (Fig. 2). A significant advancement in the onset dates of both events was observed for all species except Betula platyphylla, which showed a non-significant trend toward earlier timing (P > 0.05). The rates of advancement ranged from −0.59 to −4.52 days/year for cell enlargement and −1.19 to −4.58 days/year for wall-thickening. Notably, Fraxinus mandshurica exhibited the slowest rates (−0.59 days/year and −1.19 days/year, respectively), while Tilia mandshurica showed the highest advancing rates (−4.52 days/year and −4.58 days/year, respectively).

The onset dates of cell enlargement and wall-thickening were significantly positively correlated across species (Fig. 3). However, the slopes of the regression lines varied, indicating species-specific difference in the rate of advancement for wall-thickening relative to cell enlargement. Specifically, T. mandshurica showed the fastest advancement in wall-thickening DOY, whereas F. mandshurica exhibited the slowest.

From 2019 to 2024, the unequal advancing rates of cell enlargement and wall-thickening, led to divergent changes in the interval length between these events (Table 2). The average interval ranged from 5 to 18 days across all species, with the longest interval was observed in Pinus koraiensis and the shortest in Acer triflorum. In general, the faster advancement of wall-thickening compared to cell enlargement resulted in a consistent shortening of the interval between the two events.

3.2. Effect of environmental factors on the onset of cell enlargement, wall-thickening and the interval

LMM analysis revealed that photoperiod, forcing, chilling, and precipitation were positively correlated with the timing of cell enlargement, wall-thickening and the interval between these events (Table 3). Photoperiod emerged as the primary environmental factor driving the onset of cell enlargement in these species, accounting for 53.46% of the total variation (Fig. 4). Forcing and precipitation were the second and third most influential variables, explaining 34.87% and 7.85% of the variation, respectively. In contrast, chilling contributed only 3.82%, indicating a marginal role in the model's overall explanatory power. Similarly, LMM analysis showed that the relative ranking of the environmental factors remained consistent in determining the onset of wall-thickening, although their individual contributions varied. The relative importance of photoperiod for the onset of wall-thickening (46.89%) was slightly lower compared to its role in cell enlargement (53.46%). Forcing and precipitation accounted for 43.69% and 8.98% of the variation, respectively, while chilling played an even more negligible role in explaining wall-thickening onset, contributing only 0.44%.

The relative importance of these factors was also consistent in determining the time interval between cell enlargement and wall-thickening. LMM analysis indicated that photoperiod was the primary driver of this interval, explaining 50.12% of the variation. Forcing was the second most influential factor, accounting for 40.49% of the variation, while precipitation played a lesser but still significant role (5.85%). Although chilling contributed minimally to the interval (3.54%), it remained a statistically significant factor that should not be disregarded.

Although photoperiod and temperature are critical factors influencing the time interval, our results showed that the forcing temperature and daylength required for the transition from xylem cell enlargement to wall-thickening vary considerably among tree species (Fig. 5, Fig. 6). Specifically, Populus ussuriensis exhibited the smallest difference in forcing temperature (Δforcing temperature) between the two phases, requiring only 12 ℃, whereas Pinus koraiensis showed the largest, with a difference of up to 285 ℃ (Fig. 5). Regarding photoperiod, Tilia amurensis had the smallest Δdaylength, while P. koraiensis had the largest (Fig. 6). Notably, while daylength on a given calendar date remains constant at a fixed location, climate warming accelerates the accumulation of forcing temperature, thereby shortening the time interval between cell enlargement and wall-thickening.

4. Discussion

Analyzing the sequence of phenological events, rather than isolated occurrences, provides a more comprehensive understanding of how multiple phenological events in a given species respond to climate warming (Ettinger et al., 2018; Buonaiuto and Wolkovich, 2021; Ma et al., 2022). This approach allows for a more accurate assessment of climate change impacts at the species level (Post et al., 2008; Collins et al., 2021; Li et al., 2024). Through examining the timing of xylem cell enlargement and wall-thickening in twelve temperate tree species, we observed that these phenological events advanced for all species in response to warming. While the onset of cell enlargement and wall-thickening responded similarly to environmental factors, the extent of the response varied. Furthermore, differences in the rate of advancement between species resulted in variable changes in the interval length between these events under warming conditions. Our findings highlight that the interval between cell enlargement and wall-thickening will generally shorten for these twelve temperate tree species under climate change, with implications for tree physiology, forest productivity, and ecosystem dynamics.

4.1. Advancements in cell enlargement and wall-thickening

Climate warming has significantly altered the phenological timelines of plants, impacting forest productivity, carbon sequestration, and ecosystem services. While the phenology of primary growth events, such as leaf unfolding (Xu et al., 2021), flowering (Ma et al., 2021), fruiting (Ma et al., 2022), and leaf coloration (Li et al., 2024) has been extensively documented, research on the timing of secondary growth processes, especially in broadleaf trees, remain relatively scarce. In this study, we observed advancements in both xylem cell enlargement and wall-thickening across all species examined, although the rate of advancement varied between phenological events and species. The average rate for the conifer Pinus koraiensis was 1.32 days per year, which closely aligns with that reported for Picea mariana in boreal Canada (1.24 days per year; Rossi et al., 2011). In contrast, the broadleaf species in our study generally exhibited higher advancement rates (Fig. 2), reaching up to 4.52 days per year in Tilia mandshurica, which exceeds those reported in previous studies. For instance, Quercus pubescens advanced by 1.85 days per year in Slovenia (Gričar et al., 2022), and Betula pendula showed an average rate of 3.54 days per year in Western Europe (Dox et al., 2022). These relatively high advancement rates observed in certain broadleaf species may reflect species-specific phenological sensitivity to warming rather than a generalized response across temperate forests. The magnitude of advancement is likely influenced by the interplay between regional warming intensity and intrinsic species traits. Environmental records indicate that mean spring temperatures at our study site increased by approximately 2.2 ℃ over the five-year period, likely accelerating the accumulation of forcing temperatures and driving earlier xylem development (Ma et al., 2018; Delpierre et al., 2019). However, over extended timescales, the rates of advancement for both cell enlargement and wall-thickening are expected to decelerate (Huang et al., 2023). Photoperiod constraints and incomplete winter chilling may modulate these temperature-driven effects, especially for late-successional or photoperiod-sensitive species (Fu et al., 2015; Vitasse et al., 2018; Delpierre et al., 2019). This may partially explain the relatively high advancement observed in T. mandshurica, despite experiencing similar warming exposure as other species. Furthermore, we found a positive correlation between the timing of cell enlargement and wall-thickening, suggesting that earlier initiation of cell enlargement strongly influence the timing of wall-thickening (Cuny et al., 2015; Huang et al., 2023). For instance, Kraus et al. (2016) observed that the average start date of wall-thickening in spruce was 15 days after cell enlargement.

In addition, earlier leaf unfolding observed in concurrent phenological datasets may have contributed to earlier xylem development by advancing carbon supply, as secondary and primary growth are tightly interconnected (Huang et al., 2014; Dox et al., 2022; Qian et al., 2024a). These phenological shifts carry important physiological and ecological implications. Advancing cell enlargement and wall-thickening could enhance early-season stem growth, increase the potential for annual biomass gain, and affect intra-annual carbon allocation strategies (Petit et al., 2018; Blumstein et al., 2024). However, earlier xylem development may also increase exposure to spring frost and disrupt the synchronization between cambial activity and resource availability (Gao et al., 2022). In broadleaf species, where xylem development is tightly coupled to leaf phenology (van der Maaten et al., 2018; Grossiord et al., 2022), such mismatches may compromise tree structural integrity and reduce forest resilience under climate change. Therefore, understanding the interdependence of primary and secondary growth is critical for predicting how trees will adapt to changing environmental conditions.

4.2. Environmental drivers of cell enlargement and wall-thickening

We explored the key drivers of cell enlargement and wall-thickening by assessing four potential predictor factors (Photoperiod, forcing, chilling, and precipitation) using LMMs. The results indicated that photoperiod is the primary factor inducing the onset of both cell enlargement and wall-thickening, although its relative importance was lower for wall-thickening compared to cell enlargement. This finding aligns previous studies showing that the critical photoperiod is the dominant cue for growth onset in temperate and boreal trees (Way and Montgomery, 2015; Ding et al., 2021). Changes in photoperiod influence the synthesis and distribution of key plant hormones, such as auxins and gibberellins, which regulate cell division rates (Brackmann et al., 2018). As daylight hours increase in spring, auxins and gibberellin levels rise, stimulating cambial cell division and xylem development (Bhalerao and Fischer, 2014; Singh et al., 2017). Relative importance analysis revealed that photoperiod had a weaker influence on wall-thickening compared to cell enlargement. We hypothesize that the relative importance of photoperiod diminishes as lignification progresses, with trees increasingly rely on metabolic energy supply, where temperature and water availability become more critical (Keen et al., 2022; Muffler et al., 2024).

Forcing temperature was identified as the second important factor driving these phenological events, consistent with previous studies on various conifer species across the Northern Hemisphere (Delpierre et al., 2019; Huang et al., 2020). Trees typically require sufficient exposure to forcing temperatures to transition from dormancy to active growth, with this threshold varying among species and phenological phases (Chuine and Beaubien, 2001; Richardson et al., 2018). Relative importance analysis revealed that forcing temperature explained more variation in the timing of wall-thickening compared to cell enlargement (Fig. 4), providing further evidence that later phenological events are more temperature-sensitive (Ma et al., 2018; Li et al., 2024). Although chilling played only a marginal role in explaining the timing of phenological events, its influence should not be disregarded. Chilling primarily exerted its effects primarily by increasing the requirement of forcing temperatures (Ma et al., 2022; Huang et al., 2023). A chilling-influenced heat-sum model has also highlighted the crucial roles of forcing and chilling temperatures in triggering the onset of wood formation (Delpierre et al., 2019). Additionally, total precipitation from January to the onset of cell enlargement and wall-thickening was third important factor, after photoperiod and forcing. These findings align with previous studies emphasizing the importance of pre-growing season moisture availability in driving these phenological events (Balducci et al., 2013; Ren et al., 2015; Ziaco et al., 2018). Spring rehydration allows trees to recover water balance following winter water loss, facilitating cambial cell division and expansion (Turcotte et al., 2009). Our results quantify the relative importance of photoperiod, forcing, chilling, and precipitation in determining the onset of cell enlargement and wall-thickening in temperate trees, providing a mechanistic understanding of how these environmental factors differentially influence xylem phenology.

4.3. Shortened time interval and its ecological implications

Climate warming has been showed to induce earlier cambial resumption and delayed wood formation cessation, thereby extended the growing season (Huang et al., 2020; Qian et al., 2024b). However, the effects of climate warming on the time interval between phenological phases of xylem cell development remain underexplored. Our study addresses this gap by investigating the interval between the onset of cell enlargement and wall-thickening in twelve temperate tree species during 2019–2024. We found that this interval consistently shortened across all examined species, primarily due to the larger advancing rate of wall-thickening compared to cell enlargement. Assuming a fixed amount of forcing is required for the development of enlarging cells, rising temperatures accelerate the accumulation of forcing, thereby shortening the interval between cell enlargement and wall-thickening.

LMMs revealed that the interval between cell enlargement and wall-thickening was positively correlated with photoperiod, forcing, chilling, and precipitation. This correlation likely reflects the dependency of the transition from cell enlargement to wall-thickening on adequate carbohydrate supply, primarily derived from leaf photosynthesis (Chen et al., 2022; Herrera-Ramírez et al., 2023). Both photoperiod and temperature are crucial regulators of photosynthetic capacity (Stinziano and Way, 2017). In addition, relative importance analysis identified precipitation as the third most influential factor, highlighting its role in maintaining cell turgor pressure and enhancing photosynthetic efficiency, thus further influencing interval duration (Deans et al., 2019; Zhao et al., 2020). Notable, the advancement of phenological events driven by climate warming is not equal across species. Although the rate of advancement in the onset of cell wall-thickening is similar to that of cell enlargement in some species, this observation may be attributed to the limited sample size and short duration of the study (Fig. 2). In some cases, the onset of cell enlargement may advance more rapidly than wall-thickening, leading to an extended interval and increasing the risk of spring frost damage (Gao et al., 2022; Huang et al., 2023). While it is possible that the interval between these two phenological events may extend in some species, the interval is expected to shortened for most tree species under warming scenarios.

Variation in the interval among species likely reflect differences in adaptive strategies to environmental conditions. Drought-tolerant species, such as Pinus koraiensis and Phellodendron amurense, tend to be more resilient to fluctuations in precipitation while exhibiting greater sensitivity to photoperiod and forcing temperatures (Gennaretti et al., 2020; Qian et al., 2023). In contrast, species with higher water requirements, such as Acer and Tilia, rely more heavily on stable moisture availability and are more susceptible to changes in the interval duration under drought conditions (Seddon et al., 2016). Our findings further highlight species-specific responses to warming, as reflected in the differing thresholds of forcing temperature and daylength required for developmental transitions. For instance, P. koraiensis requires a large thermal sum for wall-thickening, suggesting stronger temperature sensitivity, while T. amurensis responds within a narrower thermal window and may be less phenological flexible. These interspecific differences may reshape competitive dynamics under climate change, as species initiating cell enlargement earlier or maintaining longer intervals could gain an advantage in resource utilization, potentially increasing their dominance (Matula et al., 2023). Such shifts may alter forest composition, biodiversity, and ecosystem function (Borges et al., 2024; Dupont-Leduc et al., 2024). Although our five-year dataset is limited for detecting long-term trends, it provides valuable insight into how climate drivers modulate xylem phenology. Long-term monitoring and mechanistic modeling will be crucial for understanding and forecasting wood formation responses to ongoing climate change, with important implications for forest management and carbon cycle projections.

Although this study focused on the onset of xylem cell development, understanding the cessation and overall duration of growth is equally critical. These later phenological phases determine the growing season length and ultimately influence the annual accumulation of wood biomass (Etzold et al., 2022). Research on coniferous species suggests that warming may delay growth cessation, further extending the growing season (Mu et al., 2023). However, prolonged cambial activity may also increase susceptibility to late-season stressors, such as drought-induced embolism or carbon resource depletion. In contrast, the responses of broadleaf species to these dynamics remain insufficiently studied. Future research should incorporate full-season xylogenesis monitoring, including the timing of growth cessation, to elucidate species-specific growth strategies and their implications for forest productivity in a warming climate.

5. Conclusions

This study elucidates the complex responses of xylem phenology to climate warming in temperate tree species, with a particular focus on the timing of cell enlargement and wall-thickening, as well as the time interval between these two events. Photoperiod and forcing temperature, or their interaction, emerged as the primary environmental factors regulating the onset of both cell enlargement and wall-thickening, as well as their respective intervals. Our findings indicate that while both phenological events are advancing, the advancing rate of wall-thickening was greater than that of cell enlargement, leading to a shortened interval between the two events. Climate warming accelerates the heat accumulation required for the transition from cell enlargement to wall-thickening, thereby shortening the time interval between these two developmental stages. This compression of xylem phenological intervals could have significant ecological and physiological implications, potentially affecting resource allocation, tree growth, and interspecific competition within forest communities. Although this study was conducted at a single site, our study provides not readily available xylem phenological data for twelve tree species in Changbai mountain. These findings offer mechanistic insights that can enhance predictions of wood formation dynamics under future climate scenarios and improve the accuracy of forest carbon models.

Acknowledgements

This research was supported by the Ministry of Science and Technology (No:2019FY101602). Experimental conditions for this research were provided by The Key Laboratory for Silviculture and Conservation of Ministry of Education, Beijing Forestry University. Jilin Changbai Mountain National Nature Reserve Administration provided convenience for field work.

CRediT authorship contribution statement

Nipeng Qian: Writing – original draft, Methodology, Conceptualization. Linxu Wang: Methodology, Formal analysis. Gangdun Li: Investigation, Formal analysis. Chunchao Dong: Methodology, Investigation. Zhenzhao Xu: Writing – review & editing, Investigation. Qijing Liu: Resources, Funding acquisition. Guang Zhou: Methodology.

Data availability

The data that support the findings of this study are openly available in the Dryad Digital Repository at http://datadryad.org/share/0OxZLC.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.