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Article

Intra-Annual Growth and Its Response to Climatic Factors of Two Salix Species under Warm Temperate Environment

College of Horticulture and Plant Protection, Henan University of Science and Technology, Luoyang 471003, China
*
Author to whom correspondence should be addressed.
Forests 2022, 13(9), 1441; https://doi.org/10.3390/f13091441
Submission received: 16 August 2022 / Revised: 2 September 2022 / Accepted: 5 September 2022 / Published: 8 September 2022

Abstract

:
Monitoring cambial activity and intra-annual growth dynamics is an effective method for identifying tree growth response to climate change. However, there have been few pieces of research on intra-annual wood formation of diffuse-porous species under monsoonal warm temperate environment. Here, we monitored weekly the cambial activity and xylem differentiation of Salix babylonica and Salix matsudana by collecting microcores during the 2018 growing season. Two willow species exhibited similar cambial activity and xylem differentiation processes, of which the onset and cessation of xylem growth was from middle/late March to early/middle November. The onset and cessation of cambial activity were slightly earlier for Salix matsudana (19 March and 12 October) than for Salix babylonica (26 March and 17 October), which peaked on 2 June and 31 May, respectively. Salix babylonica showed wider xylem increment and higher growth rate than that of Salix matsudana, of which the intra-annual xylem width was 8525 ± 1201 µm and 7603 ± 826 µm, respectively, fitted by Gompertz function. Moreover, the maximum growth rate of Salix babylonica and Salix matsudana was 79.75 μm day−1 and 66 μm day−1, respectively, occurring on 4 June (DOY155) and 26 May (DOY146). Both temperature and water availability were important factors influenced the xylem growth for two species, which Salix matsudana had a stronger response to temperature but not to water availability than Salix babylonica. These results suggested that Salix babylonica seem to grow better under moist warm temperate environment due to it being a more conservative response to the climate than Salix babylonica. These observed species-specific differences at the intra-annual scale may help researchers more accurately anticipate the species suitability in temperate forests.

1. Introduction

Forests represent a large carbon sink and their woody tissues account for 15% of annual anthropogenic CO2 emissions [1]. However, their capacity to uptake carbon as woody tissues depends on how their radial growth responds to the climate. Therefore, understanding how wood formation and radial growth occur and respond to climate at inter- and intra-annual scales is necessary for assessing the climate change potential of forests [2,3,4].
Both biotic and abiotic factors, including fire, drought, and insect outbreaks, can influence forest ecosystem and their regulating services [5,6,7], where climatic variability has a direct effect on tree growth [8]. Analytic wood and increment borer are traditional methods to study trees inter-annual growth and their relationship with climatic factors [9]. However, trees have seasonal growth pattern, thus the drivers of wood (i.e., xylem) formation and cambial dynamics at intra-annual scale may shift. Previous studies demonstrated that the rate and timing of xylem growth (xylogenesis) vary in space and time because cambial processes are predominantly controlled by temperature, moisture, or their interaction [10,11], which reflect local climatic conditions [12,13]. In cold boreal and mountainous regions, xylem growth is closely related to the seasonal course of temperature and usually exhibits a peak of growth rates around the summer solstice [14]. In semi-arid alpine forests, low spring precipitation may delay the onset of the growing season [15]. In the Mediterranean forests, due to the dry summer, growth is divided into the warm, wet spring and autumn seasons [16], and precipitation is the main driving factor that influences the tree growth [17], which leads to bimodal or even multimodal patterns in xylem growth [18]. Therefore, the level of seasonal xylem growth in response to climatic conditions may differ between different sites.
Moreover, recent research showed that, besides the site conditions, seasonal growth dynamics may also differ between forest ecosystems with different forest types (broadleaved, coniferous) [19]. In Europe and North America, intensive studies have focused on the seasonal dynamics of xylem growth, not only discussing the conifers [20] but also involving the diffuse-porous trees (birch, maple, beech, or poplar) [21,22] and ring-porous species (oak, chestnut, or ash) [23]. Michelot et al., (2012) observed clear longer growth duration for Scots pine (Pinus sylvestris), compared with that of European beech (Fagus sylvatica) and Sessile oak (Quercus petraea) under the same climatic conditions [24]. As a result, a significantly larger ring width was found for pine, which was influenced by longer growth duration. Species-specific wood anatomy structural properties (e.g., tracheid and vessel xylem) and stomata sensitivity (e.g., anisohydric and isohydric) could result in between-species different responses to climatic factors [25]. In China, most previous studies on cambial phenology were conducted in the Qinghai–Tibet Plateau [26,27], arid/semiarid region [28,29], and subtropical region [30], which referred to mainly on conifers species (e.g., Juniperus przewalskii, Picea crassifolia, Pinus massoniana) but fewer focus on broadleaf species [31]. For many species, therefore, the impacts of climate warming on xylem growth and development remain poorly understood.
Weeping willow (Salix babylonica) and Hankow willow (Salix matsudana) are deciduous broadleaved trees, and both are native willow species in China, which are currently dominant in temperate broadleaved and mixed forests of China and Europe [32,33]. The distribution ranges of these two species are almost similar, and all of them are common species used for afforestation and greening in northern China, due to its rapid growth. Salix babylonica often grows in wet areas, which are adjacent to rivers or drains, whereas Salix matsudana is more drought resistant [34,35]. At present, research of these two willows mainly focus on the cultivation technology [36]; drought tolerance [37,38]; and genetic, morphological, and physiological responses to heavy metal (Pb, Zn, Cd, etc.) and salt stress [39,40].
To the best of our knowledge, no comparative study has been undertaken into the intra-annual growth dynamics of the two or more coexisting willows used microcores and their relation to climatic factors with respect to species-specific factors, which will help to clarify the climatic signals controlling the wood formation of different willow species to improve predictions of climate warming impacts on tree growth and species’ distribution. Here, based on the xylogenesis monitoring by microcores method at biweekly/weekly intervals in 2018, we aimed (1) to characterize the dynamics of intra-annual growth (the timing of onset and end, as well as the growth rate of xylogenesis) of Salix babylonica and Salix matsudana, and (2) to relate the xylem growth with climatic variables, and further to compare the differences of the climate–growth relationship between Salix babylonica and Salix matsudana. We hypothesized that (1) both temperature and water availability may be climatic driving forces for wood formation in the transition zone from temperate zone to subtropical zone; (2) drought resistant Salix matsudana may be strongly responsive to water availability, as compared with Salix babylonica.

2. Materials and Methods

2.1. Study Site

The study was conducted on Kaiyuan Campus of Henan University of Science and Technology (34°36′ N, 112°25′ E, 142 m a.s.l., Figure 1), Central China. The site is located in warm, temperate climate, where the mean annual temperature is 14.2 °C and the annual precipitation is 598 mm from 1960 to 2017. The study year of 2018 was relatively warm and wet, with 1.1 °C higher mean annual temperature and 223 mm surplus annual precipitation than the 1960–2017 average. In the study area, the herb is dominated by Zoysia spp. and shrubs are mainly Cercis chinensis and Pittosporum tobira. The main soil type is meadow cinnamon soil.

2.2. Tree Selection and Lab Preparation

Three healthy and mature trees were randomly selected for both Salix babylonica and Salix matsudana. The diameter at breast height (1.3 m), tree height, and age of monitored Salix babylonica and Salix matsudana were 35.3 ± 1.8 cm and 25.5 ± 2 cm, 11.1 ± 0.2 m and 10.9 ± 0.4 m, and 16 ± 4 years and 13 ± 1 years, respectively.
From January to December 2018, microcores were sampled by 7–10 days intervals along the stem at breast height (1.3 m) using a Trephor [41], which is an effective tool that has been widely accepted and used in dendroecology [20]. The microcores were 2 mm in diameter and 15 mm in length, containing the previous one to three xylem rings, cambium zone, and the adjacent phloem [42]. After sampling, the microcores were immediately put in 50% ethanol and glycerol mixed solution (v:v = 1:1) and stored at 4 °C to avoid tissue deterioration [43]. A total of 180 microcores were collected. In the laboratory, the microcores were dehydrated in successive ethanol solutions (50%, 70%, 90%, 95%, and 100%), xylene, and embedded in paraffin. Transverse sections of 8 μm were cut using a Leica RM 2235 rotary microtome (Leica Microsystems, Wetzlar, Germany) and stained with 1% safranin and 0.5% fast green (in 95% ethanol) [44]. Next, the sections were observed under the Leica microscope (Leica DM 2500) to identify cambial activity and xylem differentiation.

2.3. Cambial Activity and Xylem Differentiation

In this research, cambial activity and xylem differentiation was divided into the cambial zone (CZ), radial enlargement phase (EN) and mature phase (M, Figure 2). Cambial cell was arranged in order, with thin cell wall and small cell diameter. The enlarging cell was defined as still showed thin cell walls but radial diameter was at least twice that of cambial cell. Both cambial cell and enlarging cell appeared blue-green after safranin and fast green stained [15]. Mature cell was cell wall finished the lignification, which appeared purplish red after being stained with safranin and fast green [45].
When at least one row of enlarging cell was observed, cambial activity and xylem differentiation were considered to be onset in the xylem. When no enlarging cell was observed and cell division was stopped, cambial activity was considered to have ceased. When the last cell in wall-thickening phase matured at the end of the growing period, xylem differentiation was completed [46].
For each section, the number of cells in the cambial zone was counted, and the radial growth increment of xylem was measured along three radial files using Image J [47]. For each tree, four stages were used to assess the process of xylem differentiation, including first enlarging cell, first mature cell, end of cambial activity, and completion lignifications. For each stage, differences between two species were compared by non-parametric test.

2.4. Intra-Annual Xylem Growth Fitting

To assess the dynamics of xylem growth, the xylem increment was modeled for each tree with a Gompertz function, using nonlinear regression procedure by Origin software (OriginLab Corporation, Northampton, MA, USA) [48]. The Gompertz equation was defined as:
Y = A e e k x x c
where Y is the accumulation xylem growth, x is the time expressed as DOY (day of the year), A is upper asymptote (maximum growth expressed), k is the rate of change of the shape, and xc is the date of the inflection point.
In addition, the xylem growth rate can be estimated by first-order derivation of the fitted function [49]. The maximum production rate (rmax) and the average rate of wood production (rmean) were computed as [50]:
r m a x = k A / e
r m e a n = 9 / 40 e r m a x

2.5. Climate and Growth Relationship Analysis

Daily climate data were obtained from the nearest state meteorological station in Mengjin, which was located approximately 20 km from the site (34°49′ N, 112°26′ E, 333 m a.s.l.). These data were corrected and assessed with high quality of less than 1% missing rate and nearly 100% accuracy, which could be acquired from China Meteorological Science Data Sharing Network (http://data.cma.cn) (accessed on 1 September 2020).
The effects of climate factors and tree species on the xylem growth increment and xylem growth rate were analyzed separately using linear mixed models, where the tree species and climate variables—including air mean temperature, ground surface temperature, precipitation, relative humidity, vapor pressure deficit, and sunshine duration—were designated as fixed effects, whereas individual trees were designated as random effects. All statistical analyses were conducted using R version 3.4.0 (Vienna, Austria) [51]. Daily vapor pressure deficit (VPD) was calculated from daily mean values of air temperature and relative humidity [52]. Cumulative precipitation and daily mean values of other climatic factors were calculated between two sampling intervals. Xylem growth increment and growth rate (fitting value) of each of the two sampling intervals were also calculated.

3. Results

3.1. Cambial Activity

Dynamics of the number of cambial cells in Salix babylonica and Salix matsudana showed a “single peak” during 2018 growing season (Figure 3). Salix babylonica started cambial activity at the end of March (DOY85 ± 9) and reached its maximum (12 ± 1 cells) at the end of May (DOY153 ± 9). After that, the number of cambial cells began to decline continuously until the middle of October (DOY290 ± 14). When cambial activity nearly stopped, the number of cambial cells remained at five to six. Compared with Salix babylonica, the onset and end timing of cambial activity of Salix matsudana were seven days earlier (DOY78 ± 4) and five days earlier (DOY285 ± 0), respectively. However, the timing reached the maximum value of cambial cells was two days earlier (DOY151 ± 3) than Salix babylonica, which was stable at nine to ten cells. During the dormancy in autumn, the number of cambial cells of Salix matsudana was stable at four to five, less than that of Salix babylonica.

3.2. Xylem Differentiation

Both species exhibited almost similar stem xylem differentiation process (Table 1, p > 0.05). The timing of the first mature cell in the xylem of Salix babylonica was occurred around late April (DOY111 ± 6). In the middle of November (DOY321 ± 5), the last formed xylem cell of Salix babylonica was completed. For Salix matsudana, the first mature cell appeared two days later (DOY113 ± 4) than that of Salix babylonica. After that, the last formed latewood cell finished lignification in the beginning of November (DOY311 ± 4). Correspondingly, the duration of xylogenesis was 236 days and 233 days for Salix babylonica and Salix matsudana, respectively.

3.3. Xylem Growth Comparison

The Gompertz function adequately fitted the xylem growth of Salix babylonica and Salix matsudana, which the adjusted R2 values were 0.95 and 0.88 (p < 0.001), respectively. The average width of xylem (A) was 8525 ± 1201 µm and 7603 ± 826 µm for Salix babylonica and Salix matsudana, respectively (Table 2). The average xylem width growth rate (rmean) was 48.77 μm d−1 and 40.52 μm d−1 for Salix babylonica and Salix matsudana, respectively. As excepted, the maximum xylem growth rate was 13.75 μm d−1, higher than that of Salix matsudana, and the date of maximum xylem growth rate (xc) occurred in early June (DOY155 ± 5) and late May (DOY146 ± 5) for Salix babylonica and Salix matsudana, respectively.

3.4. Climate–Xylem Growth Relationship

Both temperature (air temperature and ground surface temperature) and water availability (precipitation, relative humidity, and vapor pressure deficit) had a significant effect on the xylem growth increment for both Salix babylonica and Salix matsudana (Table 3). The xylem increments in response to water availability were similar between species. However, the effect of temperature on the width of xylem growth of Salix matsudana was stronger, compared with Salix babylonica, as indicated by the significant interaction term in the model (Table 3). The xylem growth increment of both species was not affected by sunshine duration (p > 0.05).
The xylem growth rate was also significantly affected by temperature (air temperature and ground surface temperature), water availability (precipitation and vapor pressure deficit), and sunshine duration. However, the effect of relative humidity on the growth rate was not significant. In addition, the growth rate of Salix matsudana increased more rapidly with the increase in air temperature, compared with Salix babylonica.

4. Discussion

4.1. Cambial Activity of Two Willows in Warm Temperate Zone

In this study, the onset and cessation timing of cambial activity of Salix babylonica and Salix matsudana are basically the same (Table 1), which were in the middle/late March (DOY 85 ± 9 and DOY 78 ± 4) and the middle October (DOY 290 ± 14 and DOY 285 ± 0), respectively. Correspondingly, the duration of cambial activity was 205 days and 207 days for Salix babylonica and Salix matsudana, respectively.
In Qilian Mountains, a cold and arid environment on the northeastern Tibetan Plateau, the duration of cambial activity of Juniperus przewalskii was shorter, lasting around 90 days, which started in mid-May to mid-August [27]. In the warm temperate zone, Zhang et al. reported that the duration of cambial activity of Pinus massoniana Willd lasted for about 240 days [53]. Unlike the complete dormancy of cambial cells in temperate and boreal trees, there might be a semi-dormancy in subtropical pine in January. As a result, the duration of cambial activity of Pinus massoniana in subtropical China was four or six months longer than temperate and boreal trees, which was more than 300 days [29].
It is generally considered that air temperature is the main environmental factor that controls the initiation of cambial activity. Once the daily mean air temperature reaches 6–8 °C, the tree cambium begins to be active [25]. As the seasonal average air temperature increases with decreasing latitude, an earlier onset of tree’s cambial activity along the latitude gradient is reasonable. Therefore, it could explain why in the Qilian Mountains, compared to the warm temperate zone and the subtropical zone, the onset timing of cambial activity was in mid-May, rather than mid-March or mid-February. In addition, the duration of cambial activity became longer, from approximately 90 days to 240 days, to almost all year.

4.2. Xylem Growth with High Growth Rate

Based on the measured values, the width of intra-annual xylem growth of Salix babylonica and Salix matsudana was 8203 ± 646 μm and 6616 ± 992 μm, respectively (Table 2). Similarly, the annual xylem increment of Salix matsudana at the cambial age of 12a–14a was about 7000 μm, which was analyzed by analytical wood in a semi-arid and semi-humid area [54]. By using the dendrometer method, Ma et al. found that the average annual xylem increment of Salix matsudana was 6637 μm during 2016–2019 in Beijing [55], which is in line with our findings. Although the relevant research on Salix babylonica is lacking, these studies supported that using the microcore method to monitor the intra-annual xylem growth process of willow is feasible. Additionally, the result of our work showed that Salix matsudana was in a favorable growing condition.
The growing season for both species was from March to November (Figure 4), and the daily average growth rate was 48.77 μm and 40.52 μm for Salix babylonica and Salix matsudana (Table 2), respectively, which were fitted by Gompertz model. The average growth rates of these two Salix were much higher than some trees in tropical and subtropical zones, which was 3.0 μm d−1 and 14.8 μm d−1 of Hopea pierrei in tropic and Cunninghamia lanceolata in subtropic, respectively [56,57]. This behavior could be largely explained by willow’s genetic differences, related to the species-specific capacity to fast-growing under-favorable water conditions [58]. In addition to that, tree species in warm temperate tend to complete growth during a shorter growing season but with a higher growth rate, in comparison with trees in tropical and subtropical zones.
The maximum xylem growth rate were observed around early June (DOY155 ± 5) and late May (DOY146 ± 5) for Salix babylonica and Salix matsudana, respectively, which were significantly earlier than the time of the summer solstice. It is documented for several tree species that the time at which the rate of xylem growth is peaking is synchronized with the summer solstice, especially in cold boreal forest [59,60]. This discrepancy of the timing of maximum growth rate in our result may be explained by between-sites variation in photosynthetically active radiation (PAR). In boreal forest, due to the low annual air temperature (1–3 °C), the maximum PAR has often been associated with the summer solstice when day length peaked [47]. In contrast, our study site was located in warm temperate zones, and the mean annual air temperature was considerably high with 14.2 °C (1960–2017). Thus, favorable PAR condition for tree growth can be reached before summer solstice. Additionally, the short-term drought in June 2018 (63 mm) might be another reasonable trigger for the earlier occurrence of maximum growth rate before summer solstice.

4.3. Higher Climate Growth Sensitivity in Salix matsudana Than Salix babylonica

Our results supported the first hypothesis that both temperature and water availability affected the xylem growth of two willows (Table 3). In cold climates, tree phenology is primarily controlled by temperature [30]. It is generally accepted that at high latitudes, the effect of temperature not only determines the onset of the growing season but also plays a key role for the end of the growing season [45]. However, in arid and semi-arid regions, water availability becomes a limiting factor for xylem formation [61]. Precipitation rather than temperature primarily controls xylem growth in drought-exposed trees. In warm temperate regions, both temperature and water availability might be effective climatic factors for tree growth. These variability responses of xylem growth to climatic drivers are essential to link species-specific capacity and plant-level growth phases with the environmental factors [62]. In this study, the daily mean air temperature for cambium onset and xylem growth ending of both willows was around 13.6 °C and 15.4 °C, respectively. From May to July, total precipitation was 460 mm, which accounted for 56% of the annual precipitation (Figure 5). During the same period, the width of xylem growth accounted for 67.6% of the total annual xylem increment.
Compared with Salix matsudana, Salix babylonica seemed to grow better at study site with higher xylem increment and faster growth rate. The higher sensitivity of xylogenesis in Salix matsudana to temperature may relate to inter-specific competition for Salix matsudana to adjust its growth rate than that of Salix babylonica (Table 3). On the other hand, the ecophysiological discrepancies between the two species may also explain the different xylem growth performances, of which the vessel diameter was smaller and vessel length was shorter in Salix matsudana than that of Salix babylonica [37,38]. This may result in Salix matsudana having limited plastic response in water transportation for xylem growth [34]. These findings suggest the xylem growth of Salix babylonica is clearly more conservative with respect to environmental conditions than Salix matsudana. However, conservative responses of Salix babylonica (lower sensitivity to warming temperature) may be able to minimize the growth risk better, which is caused by increasing climate warming. Therefore, when the degree of water stress imposed on the trees is released, Salix babylonica is probably competitively superior to Salix matsudana in the xylem growth at mesic site.

Author Contributions

Conceptualization, Y.Z.; methodology, Y.Z. and J.X.; validation, Y.Z. and J.X.; investigation, Y.Z. and P.L.; data curation, Y.Z., P.L., J.H. and L.Z.; writing—original draft preparation, Y.Z. and P.L.; writing—review and editing, Y.Z. All authors have read and agreed to the published version of the manuscript.

Funding

This work is funded by the National Natural Science Foundation of China (Grant No. 41801026 and 41401063), and Student Research Training Program (Grant No. 2022508).

Acknowledgments

The authors are grateful to anonymous reviewers who considerably contributed to the improvement of the manuscript.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Cuny, H.E.; Rathgeber, C.; Frank, D.; Fonti, P.; Mkinen, H.; Prislan, P.; Rossi, S.; Castillo, E.D.; Campelo, F.; Vavrík, H. Woody biomass production lags stem-girth increase by over one month in coniferous forests. Nat. Plants 2015, 1, 15160. [Google Scholar] [CrossRef]
  2. IPCC. Climate Change 2021: The physical science basis. In Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change; Cambridge University Press: Cambridge, UK, 2021. [Google Scholar] [CrossRef]
  3. Peters, R.L.; Steppe, K.; Cuny, H.E.; De Pauw, D.J.W.; Frank, D.C.; Schaub, M.; Rathgeber, C.B.K.; Cabon, A.; Fonti, P. Turgor—A limiting factor for radial growth in mature conifers along an elevational gradient. New Phytol. 2021, 229, 213–229. [Google Scholar] [CrossRef] [PubMed]
  4. Zindros, A.; Radoglou, K.; Milios, E.; Kitikidou, K. Tree line shift in the Olympus Mountain (Greece) and climate change. Forests 2020, 11, 985. [Google Scholar] [CrossRef]
  5. Anderegg, W.R.L.; Trugman, A.T.; Badgley, G.; Anderson, C.M.; Bartuska, A.; Ciais, P.; Cullenward, D.; Field, C.B.; Freeman, J.; Goetz, S.J.; et al. Climate-driven risks to the climate mitigation potential of forests. Science 2020, 368, eaaz7005. [Google Scholar] [CrossRef]
  6. Kastridis, A.; Stathis, D.; Sapountzis, M.; Theodosiou, G. Insect outbreak and long-term post-fire effects on soil erosion in Mediterranean suburban Forest. Land 2022, 11, 911. [Google Scholar] [CrossRef]
  7. Stefanidis, S.; Alexandridis, V.; Mallinis, G. A cloud-based mapping approach for assessing spatiotemporal changes in erosion dynamics due to biotic and abiotic disturbances in a Mediterranean Peri-Urban Forest. Catena 2022, 218, 106564. [Google Scholar] [CrossRef]
  8. Huang, J.G.; Ma, Q.Q.; Rossi, S.; Biondi, F.; Deslauriers, A.; Fonti, P.; Liang, E.Y.; Makinen, H.; Oberhuber, W.; Rathgeber, C.B.K.; et al. Photoperiod and temperature as dominant environmental drivers triggering secondary growth resumption in Northern Hemisphere conifers. Proc. Natl. Acad. Sci. USA 2020, 117, 20645–20652. [Google Scholar] [CrossRef]
  9. Lu, X.M.; Huang, R.; Wang, Y.F.; Sigdel, S.R.; Dawadi, B.; Liang, E.Y.; Camarero, J.J. Summer temperature drives radial growth of alpine shrub willows on the northeastern Tibetan Plateau. Arct. Antarct. Alp. Res. 2016, 48, 461–468. [Google Scholar] [CrossRef]
  10. Rossi, S.; Anfodillo, T.; Cufar, K.; Cuny, H.E.; Deslauriers, A.; Fonti, P.; Frank, D.; Gricar, J.; Gruber, A.; Huang, J.G.; et al. Pattern of xylem phenology in conifers of cold ecosystems at the Northern Hemisphere. Glob. Change Biol. 2016, 22, 3804–3813. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  11. Tumajer, J.; Shishov, V.V.; Ilyin, V.A.; Camarero, J.J. Intra-annual growth dynamics of Mediterranean pines and junipers determines their climatic adaptability. Agric. For. Meteorol. 2021, 311, 108685. [Google Scholar] [CrossRef]
  12. Delpierre, N.; Lireux, S.; Hartig, F.; Camarero, J.J.; Cheaib, A.; Cufar, K.; Cuny, H.; Deslauriers, A.; Fonti, P.; Gricar, J.; et al. Chilling and forcing temperatures interact to predict the onset of wood formation in Northern Hemisphere conifers. Glob. Change Biol. 2019, 25, 1089–1105. [Google Scholar] [CrossRef] [PubMed]
  13. Popkova, M.I.; Vaganov, E.A.; Shishov, V.V.; Babushkina, E.A.; Rossi, S.; Fonti, M.V.; Fonti, P. Modeled tracheidograms disclose drought influence on Pinus sylvestris tree-rings structure from Siberian forest-steppe. Front. Plant Sci. 2018, 9, 1144. [Google Scholar] [CrossRef] [PubMed]
  14. Chen, L.; Rossi, S.; Deslauriers, A.; Liu, J.Q. Contrasting strategies of xylem formation between black spruce and balsam fir in Quebec, Canada. Tree Physiol. 2019, 39, 747–754. [Google Scholar] [CrossRef] [PubMed]
  15. Ren, P.; Rossi, S.; Gricar, J.; Liang, E.Y.; Cufar, K. Is precipitation a trigger for the onset of xylogenesis in Juniperus przewalskii on the north-eastern Tibetan Plateau? Ann. Bot. 2015, 115, 629–639. [Google Scholar] [CrossRef]
  16. Cherubini, P.; Gartner, B.L.; Tognetti, R.; Braker, O.U.; Schoch, W.; Innes, J.L. Identification, measurement and interpretation of tree rings in woody species from Mediterranean climates. Biol. Rev. Camb. Philos. Soc. 2003, 78, 119–148. [Google Scholar] [CrossRef]
  17. Kastridis, A.; Kamperidou, V.; Stathis, D. Dendroclimatological analysis of Fir (A. borisii-regis) in Greece in the frame of climate change Investigation. Forests 2022, 13, 879. [Google Scholar] [CrossRef]
  18. Camarero, J.J.; Olano, J.M.; Parras, A. Plastic bimodal xylogenesis in conifers from continental Mediterranean climates. New Phytol. 2010, 185, 471–480. [Google Scholar] [CrossRef]
  19. Stefanidis, S.; Alexandridis, V. Precipitation and potential evapotranspiration temporal variability and their relationship in two forest ecosystems in Greece. Hydrology 2021, 8, 160. [Google Scholar] [CrossRef]
  20. Cuny, H.E.; Fonti, P.; Rathgeber, C.B.K.; von Arx, G.; Peters, R.L.; Frank, D.C. Couplings in cell differentiation kinetics mitigate air temperature influence on conifer wood anatomy. Plant Cell Environ. 2019, 42, 1222–1232. [Google Scholar] [CrossRef]
  21. Marchand, L.J.; Dox, I.; Gricar, J.; Prislan, P.; Van den Bulcke, J.; Fonti, P.; Campioli, M. Timing of spring xylogenesis in temperate deciduous tree species relates to tree growth characteristics and previous autumn phenology. Tree Physiol. 2021, 41, 1161–1170. [Google Scholar] [CrossRef]
  22. Sprengel, L.; Stangler, D.F.; Sheppard, J.; Morhart, C.; Spiecker, H. Comparative analysis of the effects of stem height and artificial pruning on seasonal radial growth dynamics of Wild Cherry (Prunus avium L.) and Sycamore (Acer pseudoplatanus L.) in a widely spaced system. Forests 2018, 9, 174. [Google Scholar] [CrossRef]
  23. Guada, G.; Vazquez-Ruiz, R.A.; Garcia-Gonzalez, I. Meteorological conditions control the cessation rather than the beginning of wood formation in a sub-Mediterranean ring-porous oak. Agric. For. Meteorol. 2020, 281, 107833. [Google Scholar] [CrossRef]
  24. Michelot, A.; Simard, S.; Rathgeber, C.; Dufrene, E.; Damesin, C. Comparing the intra-annual wood formation of three European species (Fagus sylvatica, Quercus petraea and Pinus sylvestris) as related to leaf phenology and non-structural carbohydrate dynamics. Tree Physiol. 2012, 32, 1033–1045. [Google Scholar] [CrossRef] [PubMed]
  25. Fernandez-de-Una, L.; Aranda, I.; Rossi, S.; Fonti, P.; Canellas, I.; Gea-Izquierdo, G. Divergent phenological and leaf gas exchange strategies of two competing tree species drive contrasting responses to drought at their altitudinal boundary. Tree Physiol. 2018, 38, 1152–1165. [Google Scholar] [CrossRef] [PubMed]
  26. Li, X.X.; Liang, E.; Gricar, J.; Prislan, P.; Rossi, S.; Cufar, K. Age dependence of xylogenesis and its climatic sensitivity in Smith fir on the south-eastern Tibetan Plateau. Tree Physiol. 2013, 33, 48–56. [Google Scholar] [CrossRef]
  27. Li, X.X.; Rossi, S.; Liang, E.Y.; Camarero, J.J. Temperature thresholds for the onset of xylogenesis in alpine shrubs on the Tibetan Plateau. Trees 2016, 30, 2091–2099. [Google Scholar] [CrossRef]
  28. Zhang, J.Z.; Gou, X.H.; Manzanedo, R.D.; Zhang, F.; Pederson, N. Cambial phenology and xylogenesis of Juniperus przewalskii over a climatic gradient is influenced by both temperature and drought. Agric. For. Meteorol. 2018, 260, 165–175. [Google Scholar] [CrossRef]
  29. Zhang, J.Z.; Gou, X.H.; Pederson, N.; Zhang, F.; Niu, H.G.; Zhao, S.D.; Wang, F. Cambial phenology in Juniperus przewalskii along different altitudinal gradients in a cold and arid region. Tree Physiol. 2018, 38, 840–852. [Google Scholar] [CrossRef]
  30. Huang, J.G.; Guo, X.; Rossi, S.; Zhai, L.; Yu, B.; Zhang, S.; Zhang, M. Intra-annual wood formation of subtropical Chinese red pine shows better growth in dry season than wet season. Tree Physiol. 2018, 38, 1225–1236. [Google Scholar] [CrossRef] [Green Version]
  31. Wang, L.; Gou, X.; Xia, J.; Wang, F.; Fang, F.; Zhang, J. Research progress on cambial activity of trees and the influencing factors. Chin. J. Appl. Ecol. 2021, 32, 3761–3770. [Google Scholar] [CrossRef]
  32. Rao, G.D.; Sui, J.K.; Zeng, Y.F.; He, C.Y.; Duan, A.G.; Zhang, J.G. De novo transcriptome and small RNA analysis of two Chinese willow cultivars reveals stress response genes in Salix matsudana. PLoS ONE 2014, 9, 1932–6203. [Google Scholar] [CrossRef]
  33. Tao, Z.X.; Xu, Y.J.; Ge, Q.S.; Dai, J.H.; Wang, H.J. Reduced frost hardiness in temperate woody species due to climate warming: A model-based analysis. Clim. Change 2021, 165, 35. [Google Scholar] [CrossRef]
  34. Feng, X.Y. A Comparative Study of Plant Hydraulic and Gas Exchange Traits in Salix Species. Master’s Thesis, Lanzhou University, Lanzhou, China, 2020. [Google Scholar] [CrossRef]
  35. Wu, Z.Y. Flora of China; Science Press: Beijing, China, 1999; pp. 162–274. [Google Scholar]
  36. Bhatta, S.P.; Sharma, K.P.; Balami, S. Variation in carbon storage among tree species in the planted forest of Kathmandu, Central Nepal. Curr. Sci. 2018, 115, 274–282. [Google Scholar] [CrossRef]
  37. Ogasa, M.; Miki, N.H.; Murakami, Y.; Yoshikawa, K. Recovery performance in xylem hydraulic conductivity is correlated with cavitation resistance for temperate deciduous tree species. Tree Physiol. 2013, 33, 335–344. [Google Scholar] [CrossRef] [PubMed]
  38. Wang, S.; Fan, J.; Ge, J.M.; Wang, Q.M.; Fu, W. Discrepancy in tree transpiration of Salix matsudana, Populus simonii under distinct soil, topography conditions in an ecological rehabilitation area on the northern Loess Plateau. For. Ecol. Manag. 2019, 432, 675–685. [Google Scholar] [CrossRef]
  39. Chen, Y.; Jiang, Y.; Chen, Y.; Feng, W.; Zhang, J. Uncovering candidate genes responsive to salt stress in Salix matsudana (Koidz) by transcriptomic analysis. PLoS ONE. 2020, 15, e0236129. [Google Scholar] [CrossRef]
  40. Zhang, J.; Yuan, H.W.; Yang, Q.S.; Li, M.; Wang, Y.; Li, Y.J.; Ma, X.J.; Tan, F.; Wu, R.L. The genetic architecture of growth traits in Salix matsudana under salt stress. Hortic. Res. 2017, 4, 17024. [Google Scholar] [CrossRef]
  41. Zhang, Y.P.; Xu, J.L.; Jiang, Y.; Mandra, T.; Rademacher, T.T.; Xue, F.; Dong, M.Y.; Pederson, N. Higher plasticity of water uptake in spruce than larch in an alpine habitat of North-Central China. Agric. For. Meteorol. 2021, 311, 108696. [Google Scholar] [CrossRef]
  42. Rossi, S.; Menardi, R.; Anfodillo, T. Trephor: A new tool for sampling microcores from tree stems. IAWA J. 2006, 27, 89–97. [Google Scholar] [CrossRef]
  43. Zhang, Y.P.; Xu, J.L.; Su, W.; Zhao, X.P.; Xu, X.L. Spring precipitation effects on formation of first row of earlywood vessels in Quercus variabilis at Qinling Mountain (China). Trees 2019, 33, 457–468. [Google Scholar] [CrossRef]
  44. Zhang, Y.P.; Jiang, Y.; Wen, Y.; Ding, X.Y.; Wang, B.; Xu, J.L. Comparing primary and secondary growth of co-occurring deciduous and evergreen conifers in an alpine habitat. Forests 2019, 10, 574. [Google Scholar] [CrossRef]
  45. Zhang, J.Z. Cambial Phenology and Intra-Annual Radial Growth Dynamics of Conifers over the Qilian Mountains. Ph.D. Thesis, Lanzhou University, Lanzhou, China, 2018. [Google Scholar] [CrossRef]
  46. Vavrčík, H.; Gryc, V.; Vichrová, G. Xylem formation in young Norway spruce trees in drahany highland, Czech Republic. IAWA J. 2013, 34, 231–244. [Google Scholar] [CrossRef]
  47. Rossi, S.; Deslauriers, A.; Anfodillo, T. Assessment of cambial activity and xylogenesis by microsampling tree species: An example at the alpine timberline. IAWA J. 2006, 27, 383–394. [Google Scholar] [CrossRef]
  48. Deslauriers, A.; Morin, H.; Begin, Y. Cellular phenology of annual ring formation of Abies balsamea in the Quebec boreal forest (Canada). Can. J. For. Res. 2003, 33, 190. [Google Scholar] [CrossRef]
  49. Jiang, Y.; Zhang, Y.P.; Guo, Y.Y.; Kang, M.Y.; Wang, M.C.; Wang, B. Intra-annual xylem growth of Larix principis-rupprechtii at its upper and lower distribution limits on the Luyashan mountain in North-Central China. Forests 2015, 6, 3809–3827. [Google Scholar] [CrossRef]
  50. Rathgeber, C.B.K.; Rossi, S.; Bontemps, J.D. Cambial activity related to tree size in a mature silver-fir plantation. Ann. Bot. 2011, 108, 429–438. [Google Scholar] [CrossRef]
  51. R Development Core Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2015. [Google Scholar]
  52. Bauman, D.; Fortunel, C.; Delhaye, G.; Malhi, Y.; Cernusak, L.A.; Bentley, L.P.; Rifai, S.W.; Aguirre-Gutiérrez, J.; Menor, I.O.; Phillips, O.L.; et al. Tropical tree mortality has increased with rising atmospheric water stress. Nature 2022, 608, 528–533. [Google Scholar] [CrossRef]
  53. Zhang, S.K.; Huang, J.G.; Rossi, S.; Ma, Q.Q.; Yu, B.Y.; Zhai, L.H.; Luo, D.W.; Guo, X.L.; Fu, S.L.; Zhang, W. Intra-annual dynamics of xylem growth in Pinus massoniana submitted to an experimental nitrogen addition in Central China. Tree Physiol. 2017, 37, 1546–1553. [Google Scholar] [CrossRef]
  54. Wang, Q.B.; Qiao, H.B.; Zhang, D. Expected maturity age of individual Salix matsudana. Prot. For. Sci. Technol. 2014, 12, 24–25. [Google Scholar] [CrossRef]
  55. Ma, X.D.; Pang, Z.; Wu, J.Y.; Zhang, G.F.; Dai, Y.C.A.; Zou, J.L.; Kan, H.M. Seasonal pattern of stem radial growth of Salix matsudana and its response to climatic and soil factors in a semi-arid area of North China. Glob. Ecol. Conserv. 2021, 28, e01701. [Google Scholar] [CrossRef]
  56. Huang, Y.Q.; Deng, X.W.; Zhao, Z.H.; Xiang, W.H.; Yan, W.D.; Ouyang, S.; Lei, P.F. Monthly radial growth model of Chinese Fir (Cunninghamia lanceolata (Lamb.) Hook.), and the relationships between radial increment and climate factors. Forests 2019, 10, 757. [Google Scholar] [CrossRef]
  57. Pumijumnong, N.; Danpradit, S.; Tadang, N.; Buajan, S.; Muangsong, C. Cambial activity and radial growth dynamics of three tropical tree species at Chang Island, Thailand. J. Trop. For. Sci. 2019, 31, 404–414. [Google Scholar] [CrossRef]
  58. Liu, T.D.; Jiang, K.; Tan, Z.Y.; He, Q.F.; Zhang, H.; Wang, C. A method for performing reforestation to effectively recover soil water content in extremely degraded tropical rain forests. Front. Ecol. Evol. 2021, 9, 643994. [Google Scholar] [CrossRef]
  59. Rossi, S.; Girard, M.J.; Morin, H. Lengthening of the duration of xylogenesis engenders disproportionate increases in xylem production. Glob. Change Biol. 2014, 20, 2261–2271. [Google Scholar] [CrossRef] [PubMed]
  60. Saderi, S.; Rathgeber, C.B.K.; Rozenberg, P.; Fournier, M. Phenology of wood formation in larch (Larix decidua Mill.) trees growing along a 1000 m elevation gradient in the French Southern Alps. Ann. For. Sci. 2019, 76, 89. [Google Scholar] [CrossRef]
  61. He, M.; Yang, B.; Wang, Z.; Bruning, A.; Pourtahmasi, K.; Oladi, R. Climatic forcing of xylem formation in Qilian juniper on the northeastern Tibetan Plateau. Trees 2016, 30, 923–933. [Google Scholar] [CrossRef]
  62. Vieira, J.; Carvalho, A.; Campelo, F. Tree growth under climate change: Evidence from xylogenesis timings and kinetics. Front. Plant Sci. 2020, 11, 90. [Google Scholar] [CrossRef] [Green Version]
Figure 1. Geographical location of study site in central China (a,b), the study area landscape from Google Earth (c), and the photos of two tree species (d,e). Species photos were taken by Pengfei Luo.
Figure 1. Geographical location of study site in central China (a,b), the study area landscape from Google Earth (c), and the photos of two tree species (d,e). Species photos were taken by Pengfei Luo.
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Figure 2. Phases of wood formation of Salix babylonica (a,c) and Salix matsudana (b,d) in 2018. (a,b): on 10 March, no new xylem cell production was observed and the cambial zone (CZ) consisted of five to six cells and four to five cells for Salix babylonica (a,c) and Salix matsudana, respectively. (c,d): In the middle of the growing season (4 May) enlarging (EN), wall-thickening (WT), and mature (M) cells in xylem. Scale bar = 100 μm.
Figure 2. Phases of wood formation of Salix babylonica (a,c) and Salix matsudana (b,d) in 2018. (a,b): on 10 March, no new xylem cell production was observed and the cambial zone (CZ) consisted of five to six cells and four to five cells for Salix babylonica (a,c) and Salix matsudana, respectively. (c,d): In the middle of the growing season (4 May) enlarging (EN), wall-thickening (WT), and mature (M) cells in xylem. Scale bar = 100 μm.
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Figure 3. Number of cells observed in the cambial zone of Salix babylonica and Salix matsudana during 2018. Dots and bars represent average number of cells and standard deviations among three trees, respectively.
Figure 3. Number of cells observed in the cambial zone of Salix babylonica and Salix matsudana during 2018. Dots and bars represent average number of cells and standard deviations among three trees, respectively.
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Figure 4. (a,b) Intra-annual xylem growth dynamics and (c,d) the daily growth rate of Salix babylonica and Salix matsudana. Dots and lines represent the measured value and fitted value by the Gompertz function, respectively.
Figure 4. (a,b) Intra-annual xylem growth dynamics and (c,d) the daily growth rate of Salix babylonica and Salix matsudana. Dots and lines represent the measured value and fitted value by the Gompertz function, respectively.
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Figure 5. Intra-annual xylem growth of Salix babylonica and Salix matsudana fitted by Gompertz function and the corresponding main climatic factors during 2018 growing season.
Figure 5. Intra-annual xylem growth of Salix babylonica and Salix matsudana fitted by Gompertz function and the corresponding main climatic factors during 2018 growing season.
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Table 1. Xylem differentiation of Salix babylonica and Salix matsudana.
Table 1. Xylem differentiation of Salix babylonica and Salix matsudana.
First Enlarging CellFirst Mature CellEnd of Cambial ActivityCompletion Lignification
Salix babylonica85 ± 9111 ± 6290 ± 14321 ± 5
Salix matsudana78 ± 4113 ± 4285 ± 0311 ± 4
z−0.943−0.471−0.696−1.65
p0.3460.6530.4870.099
Date was expressed as day of the year (DOY).
Table 2. Measured and fitted values of radial growth increment in 2018.
Table 2. Measured and fitted values of radial growth increment in 2018.
Measured Value (μm)A (μm)rmean (μm/d)rmax (μm/d)xc (DOY)
Salix
babylonica
17870715445.5974.54150
29106 47.4877.64161
37634834253.2587.07153
Salix
matsudana
17742863634.5356.45153
26778756037.9862.10145
35329661449.0580.20140
A = upper asymptote (maximum growth), rmean = the mean radial growth rate, rmax = the maximum radial growth rate, xc = the date of the maximum growth rate occurrence (the inflection point), DOY = day of the year. The fitted values (A, rmean, rmax and xc) were modeled by Gompertz function.
Table 3. Effects of daily climate factors on the xylem growth increment and xylem growth rate of Salix babylonica and Salix matsudana. In the models, Salix babylonica represents the reference group.
Table 3. Effects of daily climate factors on the xylem growth increment and xylem growth rate of Salix babylonica and Salix matsudana. In the models, Salix babylonica represents the reference group.
Model ParametersXylem Growth IncrementXylem Growth Rate
EstimateSEt-ValueEstimateSEt-Value
Air temperature
     Intercept−153.3140.04−3.83 ***−12.155.70−2.13 *
     Ta21.652.0210.74 ***2.220.297.75 ***
     S. matsudana−119.3156.62−2.11 *−12.468.06−1.55
     Ta × S. matsudana8.132.852.85 **0.820.412.03 *
Ground surface temperature
     Intercept−124.81 41.12 −3.04 **−10.68 5.52 −1.94
     GST17.87 1.83 9.77 ***1.91 0.25 7.77 ***
     S. matsudana−105.14 58.16 −1.81−11.32 7.80 −1.45
     GST × S. matsudana6.55 2.59 2.53 *0.68 0.35 1.95
Precipitation
     Intercept158.99 28.14 5.65 ***23.42 3.70 6.32 ***
     PRE3.41 0.73 4.66 ***0.22 0.10 2.26 *
     S. matsudana−6.04 39.80 −0.15−0.33 5.24 −0.06
     PRE × S. matsudana1.44 1.04 1.390.12 0.14 0.87
Relative humidity
     Intercept4.33 102.01 0.0423.40 12.60 1.86
     RH398.63 161.96 2.46 *9.40 20.00 0.47
     S. matsudana−77.97 144.29 −0.54−4.44 17.82 −0.25
     RH × S. matsudana178.89 229.05 0.7811.81 28.29 0.42
Vapor pressure deficit
     Intercept110.24 50.28 2.19 *5.84 5.48 1.06
     VPD151.74 62.57 3.08 **25.51 5.38 4.74 ***
     S. matsudana−17.66 71.11 −0.25−4.67 7.76 −0.60
     VPD × S. matsudana54.12 69.67 0.788.18 7.60 1.08
Sunshine duration
     Intercept132.77 65.75 2.02 *7.34 7.51 0.98
     SSD17.90 9.46 1.893.36 1.08 3.11 **
     S. matsudana14.12 92.98 0.150.91 10.61 0.09
     SSD × S. matsudana2.73 13.38 0.200.29 1.53 0.19
* p < 0.05; ** p < 0.01; *** p < 0.001.
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Zhang, Y.; Luo, P.; Xu, J.; Hou, J.; Zhai, L. Intra-Annual Growth and Its Response to Climatic Factors of Two Salix Species under Warm Temperate Environment. Forests 2022, 13, 1441. https://doi.org/10.3390/f13091441

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Zhang Y, Luo P, Xu J, Hou J, Zhai L. Intra-Annual Growth and Its Response to Climatic Factors of Two Salix Species under Warm Temperate Environment. Forests. 2022; 13(9):1441. https://doi.org/10.3390/f13091441

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Zhang, Yiping, Pengfei Luo, Junliang Xu, Jiayu Hou, and Lexin Zhai. 2022. "Intra-Annual Growth and Its Response to Climatic Factors of Two Salix Species under Warm Temperate Environment" Forests 13, no. 9: 1441. https://doi.org/10.3390/f13091441

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