- Research Paper
Extended xylogenesis and stem biomass production in Juniperus przewalskii Kom. during extreme late-season climatic events
Annals of Forest Science volume 77, Article number: 99 (2020)
Late-season extreme climatic events induced variations in wood density and extended growth for more than a month in 2016 in Juniperus przewalskii Kom. growing on the Northeastern Tibetan Plateau, suggesting extraordinary growth resilience of the species in response to short extreme events over the cold and arid region.
Monitoring xylem formation (xylogenesis) during extreme meteorological events helps assessing climate change impacts on tree growth.
For better insight into tree-growth responses, here we compare the intra-annual formation of annual ring with and without intra-annual density fluctuation in J. przewalskii in a cold and arid environment on the Northeastern Tibetan Plateau.
Cambial phenology and xylogenesis observations of five mature trees during the 2016 intra-annual density fluctuation growth ring and the five-preceding year (2011–2015) were used for comparison. The frequency of population level occurrence of intra-annual density fluctuation in 2016 was examined on additional 50 randomly selected trees.
The return of precipitation in conjunction with warm temperatures after summer drought promoted the growth resumption in 64% of our study trees, resulting in the observed intra-annual density fluctuation. These trees experienced a growing season 1 month longer than trees without intra-annual density fluctuation. The extended growth period resulted in a 17% increase in stem biomass in trees that experienced intra-annual density fluctuation.
Our results highlight the extraordinary resilience of J. przewalskii trees in response to extreme climatic events in the cold and dry conditions of the Tibetan Plateau.
Understanding how intra-annual tree growth responds to transient extreme meteorological events is important to better assess the impacts of future climate on tree growth (Fonti et al. 2010). The timing and duration of tree growth and the structure of the annual ring are environmental sensitive and thus respond to a large range of biotic and abiotic factors, including variations in temperature, precipitation, and extreme weather events (Deslauriers et al. 2017). Resolving the immediate tree response to weather conditions is timely also considering that climate projections suggesting important growing seasons shift and extensions due to climate warming (Rossi et al. 2016; Sanchez-Salguero et al. 2017). In addition, some regions could face alteration of the precipitation regimes with more frequent, intense, or longer droughts (Kumagai et al. 2004). Tree growth has been observed to be highly malleable in response to changing environmental conditions (Deslauriers et al. 2017), but it is not fully evident that trees in today’s forests are resilient (adjust their growth to resume wood production) to the extreme weather conditions expected in the future. Studies that address these uncertainties via observations at the cellular level could have profound implications for a better mechanistic understanding of the growth processes. The consequences of such insight range from tree survival, species distributions, and the global carbon cycle (Fang et al. 2001; Pan et al. 2011).
Trees can respond to extreme climatic and weather events through a variety of structural adjustments or alterations of physiological processes. Some adaptations in the canopy include canopy dieback (McDowell and Allen 2015), changes in leaf function, or early leaf fall (Fernandez-de-Una et al. 2017). Some adaptations occur in the mechanisms that regulate stem growth (wood formation), including compensation for a shorter growing season with increased rates of cell production (Balducci et al. 2016; Cuny et al. 2019), decreasing the number of latewood cells (Wang et al. 2000), ceasing growth on one or more sides of the stem (Novak et al. 2016), or the cessation of cellular division under extreme water deficit (Deslauriers et al. 2016; Zhang et al. 2018). These kinds of plastic responses to extreme weather events in the cambium are reflected in the layering of xylem cells in radial growth rings through the number of cells produced or the anatomy of cells within a growth ring. When unfavorable climatic conditions occur, such as a severe summer drought, trees may initiate latewood cell formation (smaller lumen and thicker cell walls) well before the end of the growing season, reducing or even stopping cell division (Deslauriers et al. 2016). If there is a return of favorable conditions, trees can resume the production of earlywood-like tracheids with larger lumina and thinner walls (De Micco et al. 2016b). This intra-seasonal layering of earlywood-like tracheids after the creation of latewood tracheids, referred to as “false rings” (Schulman 1939) or intra-annual density fluctuations (IADFs), reflects important physiological processes and mechanical structures of tree responses to strong exogenous stimuli (De Micco et al. 2016b).
IADF formation has been frequently studied in the Mediterranean region where it is a common occurrence (De Micco et al. 2016b). Studies there have classified IADFs into two main types according to their relative position, within either the earlywood (E-type) or latewood (L-type) (Campelo et al. 2007; De Micco et al. 2016b). While E-type IADFs are related to conditions of extreme drought and high temperatures during the growing season, L-type IADFs are formed when the cambium reactivates under favorable late growing season conditions (Campelo et al. 2007; De Micco et al. 2016b). L-type IADF formation results in an extension of the wood formation period. Although IADFs have been observed in different environments around the world (Copenheaver et al. 2006; De Grandpré et al. 2011; Edmondson 2010; Marchand and Filion 2012; Masiokas and Villalba 2004), reports of IADF formation and potential formation mechanisms are much less frequent outside of the Mediterranean region. Therefore, further studies are needed to increase our understanding of IADF formation in other environments.
Most studies of IADFs have been conducted indirectly through the extraction of growth rings by increment coring, where correlations are made between years with the presence of IADFs and a range of climate variables (Battipaglia et al. 2016; Campelo et al. 2007). While these studies can identify the potential conditions or extreme climatic events leading to IADF formation, interpretations of what drives IADF formation can be uncertain. By sampling tree stems every 1–2 weeks, so-called microcoring, researchers can more precisely identify periods of cell production throughout the growing season (Fonti et al. 2010). Microcoring, therefore, provides better insight into the precise timing of xylogenesis and a more direct and precise temporal investigation of what drives IADF formation (De Micco et al. 2016a). A few studies have applied these direct and frequent observations of xylogenesis to investigate IADF formation (Balzano et al. 2018; De Micco et al. 2016a). However, there is still much to learn about how other tree species and other environments respond to changes in the timing and structure of the growing season and extreme weather events in many different tree species and in many of the world’s forests.
In this study, we monitored the formation of the annual rings of Juniperus przewalskii Kom. trees during 2011–2016 with and without IADF formation in a cold and arid environment on the northeastern Tibetan Plateau. Specifically, we intend to (1) characterize the process of IADF formation, (2) identify its main drivers, and (3) assess its frequency of occurrence and (4) potential impacts on biomass productivity. We tested the hypothesis that the IADF formation in J. przewalskii, like observed in some Mediterranean species, is a plastic response mechanism to favorable growth conditions that follow an unfavorable period.
2 Materials and methods
2.1 Study site
Our study site is located at 3100 m above sea level (asl) in the Tulugou National Forest Park (36° 43′ 21″ N, 103° 37′ 59″ E) of the northeastern Tibetan Plateau (Fig. 1a). As recorded by an on-site meteorological station (HOBO U30, Onset, USA) from 2011 to 2016, local climate is characterized by a mean annual temperature of 1.7 °C and an annual precipitation sum of 699 mm, indicating an arid and cold climate (Fig. 1b). Our study forest is composed of J. przewalskii trees growing at the upper forest limit on a dry, infertile, and south-facing slope. Our study trees are mature, 6 to 9 m tall, and have a stem diameter at breast height (DBH) between 15 and 30 cm. As typical for steppe forests, canopy cover is less than 20%.
2.2 Microcore collection, preparation, and observation
Observations of xylem development were performed of five dominant mature trees without substantial damages or anomalies. Selected trees were upright, 64 ± 7 years old, 6.3 ± 0.5 m tall, and displayed an average DBH of 24.2 ± 3.0 cm. Observations were based on repeated microcoring using a Trephor (Rossi et al. 2006). Microcores were taken at stem breast height (1.3 m) weekly (2011–2014) or biweekly (2015–2016) from mid-April until the end of September. Three microcores were taken from each tree in each sampling date (see Zhang et al. 2018 for details). Immediately after collection, microcores were stored in a solution of formalin, alcohol, and acetic acid on a 5:90:5 ratio. In the laboratory, microcores were softened in 70% alcohol and glycerin solution (1:1), dehydrated in ethanol, cleaned in dimethylbenzene, and embedded in paraffin. Transverse sections of 12-μm thickness were cut with a rotary microtome (RM 2245, Leica, Germany), stained with safranin (1% in water) and fast green (0.5% in 95% ethanol), and photographed under an optical microscope at 100–400 of magnification (bright field and polarized light).
We counted the number of cambial, enlargement, wall thickening, and mature cells on each micro-section along three radial rows. Cambial cells had rectangular shape, small radial diameters, and thin primary walls. During the enlargement phase, cells were at least two times larger than cambial cells and had thin walls that were not birefringent under polarized light. Wall thickening cells were distinguished by the birefringence of the oriented microfibrils within the secondary walls under polarized light (Abe et al. 1997). Mature cells had lignified walls without protoplasts, and the walls were completely stained red by saffron and fast green counterstaining (Zhang et al. 2013).
Xylem development was characterized via timing of relevant phenological phases. Specifically, we annotated the day of the year (DOY) corresponding to the onset and cessation of cell enlargement (here defined as duration of cell production) and the end of cell maturation (corresponding to the end of xylogenesis). However, since we observed a bimodal growth with formation of IADF in 2016, we also annotated the second onset and ending of cell enlargement in IADF trees (i.e., corresponding to the second growing mode). The daily mean growth rate was simply calculated as the ratio of the total number of xylem cells produced during the growing season and the duration of cell production.
2.3 IADF occurrence
To assess the occurrence of IADF at the population level, we made a collection of tree-core samples from 50 randomly selected trees around our microcored trees using an increment borer in 2018. Core samples were extracted at breast height (1.3 m) from each tree in four different directions. All the samples were mounted, air-dried, and sanded to facilitate annual ring identification (Stokes and Smiley 1968). Rings were crossdated and IADFs were identified under a microscope. Total ring width and the ring width before IADF formation in 2016 were measured to the nearest 0.001 mm using a Velmex measuring system. The ring width after IADF formation was calculated as the difference between the total ring width and the width before IADF formation. The boundary between the IADF was defined as the location with a sudden change in cell size, lumen size, and color. DBHs were also collected from all cored trees.
2.4 Meteorological data
To identify the driving climatic factors inducing IADF, we used daily data from the on-site meteorological station recording air temperature, precipitation, relative humidity, soil temperature, and soil water content at 10-cm depth at 10-min resolution from 2011 to 2016.
2.5 Stem biomass estimation
To estimate the additional stem biomass associated with the IADF formation, we used allometric equations to assess the amount of wood produced in the year 2016. Because there were no reported allometric equations for J. przewalskii, we estimated the stem biomass (Bst) using the allometric equation for a species with similar architecture, Juniperus thurifera (García Morote et al. 2012):
The stem biomass associated with IADF formation was estimated as the difference between total of biomass with the growth and before IADF formation:
where BstIADF is the stem biomass associated with IADF formation, rwb indicates the ring width before IADF formation, and rwt means the total ring width of 2016.
3.1 The climatic peculiarity of the 2016 growing season
In 2016, both mean annual temperature and total precipitation were slightly higher than those in the previous 5 years (2.2 °C in 2016 versus an average of 1.6 °C from 2011 to 2015 and 732.2 mm in 2016 versus an average of 692 mm from 2011 to 2015, respectively). However, the distribution of precipitation during the 2016 growing season was substantially different. In 2016, there was no precipitation for the 16 days between July 29 and August 13 (DOY 211-226), resulting in the lowest soil water content of the growing season (Fig. 2a). At the same time, average mean temperature during the 16-day drought was higher than any measured mean from 2011 to 2015 (15.5 °C in 2016 versus a mean of 12.3 °C from 2011 to 2015). The warm and dry period of 2016 ended on August 14 (DOY 227) with the largest amount of daily precipitation (30.8 mm) of the year. After the downpour of August 14, the following 38 days saw relatively large and rather frequent rainfall events, which made September 2016 the wettest month of the year. At the same time, daily mean temperatures did not drop below 6.1 °C until September 19 (DOY 262). Previously, the date when daily mean temperature first dropped below 6.1 °C from 2011 to 2015 ranged from Sept. 1 in 2012 to Sept. 14 in 2014. The meteorological we collected underscore that 2016 was an unusually dynamic late season compared to the previous 5 years at our study site.
Although the timing and duration of xylogenesis varied significantly among the first 5 years (2011–2015) (Fig. 2b), the period of cell production typically occurred between May 2 (DOY 122, in 2013) and August 4 (DOY 216, in 2011), and tracheid maturation maximally extended to September 7 (DOY 250, in 2011). The longest duration of cell production was in 2011 and covered 79 days (from May 18 to August 4 (DOY 138-216)) while 2012 showed the shortest duration of cell production (55 days from May 28 to July 21 (DOY 149-203)). When including the period of maturation, the longest observed growing season was also in 2011 (113 days, from May 18 to September 7 (DOY 138-250)). The shortest observed growing season (87 days) occurred in 2014 and lasted from May 22 to August 16 (DOY 142-228).
Xylogenesis in 2016 showed a different pattern than compared to the previous 5 years. Two trees followed the patterns and timing of xylogenesis observed during the previous 5 years. However, three trees showed a bimodal growth pattern that included the formation of IADF and an extended growing season (Fig. 3). The onset of cell production in 2016 for all five trees was rather synchronous and started around May 18 (DOY 139) (Figs. 2b and 4). And, like the two trees without IADF, cell production of the three IADF trees was complete by August 3 (DOY 216). From there, the xylogenesis of these two populations diverged. While all xylem cells in the two non-IADF trees matured by September 2 (DOY 246, Fig. 4(b)), the three IADF trees showed new growth, the production of earlywood-like enlarging, and wall thickening cells on August 16 (DOY 229, Fig. 4(b, c)). Based on our samples and analyses, one can logically conclude that IADFs developed in these trees sometime between August 3 and August 16 (Figs. 2–4). The season of cell production in the trees with IADF formation was completed between September 2 (DOY 246) and September 13 (DOY 257), which is more than a month later than the two non-IADF trees. Termination of cell wall lignification in the three trees with IADF formation occurred around our last sampling date, September 30.
Even though peak cell production in both trees with and without IADFs occurred in early June (DOY 167), a comparison of phases in cell developmental between these groups indicated a higher number of cambial cells (Fig. 4) and a significantly higher mean rate of cell production in IADF trees than in non-IADF trees (Fig. 5b). Both groups also stopped cell division (i.e., the number of enlargement cells dropped to zero) by August 3 (Figs. 3 and 4). Cell division resumed in the IADF trees where an average of 2.4 ± 0.8 enlarging earlywood-like cells and 1.7 ± 0.1 latewood-like cells was observed among the three trees on August 16 and September 2, respectively. The number of wall-thickening cells was higher in IADF trees than in non-IADF trees before August 3, when all the trees first stopped cell production.
The total number of xylem cells produced each year was variable over the course of our 6 years of observation. The highest level of cell production occurred in 2012 and reached a mean of 42 cells, which is twice the value for 2015, which registered only a mean of 21 cells (Zhang 2018). Notably for 2016 and much like the minimum and maximum values of xylem cell production over our 6 years of observations, trees with IADFs showed a high total number of produced xylem cells that was approximately twice that of non-IADF trees (39 ± 6 cells vs. 21 ± 5 cells).
3.3 IADF occurrence and extra biomass production
Our tree-coring campaign in the forest surrounding our five micro-cored trees showed that 32 out of 50 trees formed IADFs within the 2016 annual growth ring (Table 2). This proportion (64%) confirms the rate of IADF formation observed on the xylogenesis trees (60%). Similar to findings in the micro-cored trees, increment-cored trees with IADFs had a higher mean growth rate, and produced more cells (Fig. 5a–c) and a wider 2016 ring (Fig. 5d) than non-IADF trees. Interestingly, the average DBH of trees with IADFs was slightly smaller than that of non-IADF trees, both in micro-cored trees and in increment-cored trees (Fig. 5a).
The extra growth observed in trees with IADFs resulted in extra biomass production. Micro-cored IADF trees, with a mean of 5.3 ± 0.5 additional xylem cells, yielded a mean radial increase of 169 ± 17 μm and a mean increase of 17.2 ± 4.3% of xylem cells (Table 1). Similarly, a mean of 161 ± 58 μm of additional ring width was measured in the 32 increment-cored trees with IADFs in 2016. This additional IADF-related growth resulted in a mean increase of 17.4 ± 9.5% of radial increment (Table 2). Translating IADF-related growth into biomass showed a net increase of 0.14 ± 0.02 kg, which corresponds to a + 18.1 ± 4.7% of wood production in micro-cored trees (Table 1, Fig. 6). Similar values were calculated for the 32 increment-cored IADF trees (0.12 ± 0.06 kg, i.e., +16.9 ± 8.7%; Table 2, Fig. 6).
Our observations indicated that 60–64% of J. przewalskii trees in our study forest showed a resumption of cambial growth after a growth cessation in August 2016. The bimodal growth pattern resulted in annual rings that contained variations in cell structure and wood density within the latewood of the growth ring, aka, L-type IADFs (Campelo et al. 2007). To the best of our knowledge, this is the first time that this kind of post-growing season L-type IADF formation has been observed in continental environment as cool and dry as the Tibetan Plateau. Remarkably, we observed that a majority of the study population trees were able to extend cambial growth for more than a month longer than previously observed.
4.1 Potential cause of IADF formation
Two processes are required to generate an IADF. The first is a slow-down or cessation in the processes driving cambial growth. The second is a resumption of growth after the initial cessation (Popkova et al. 2018; Vieira et al. 2014). In this study, we observed a reduction of cell production concurrent with the warm dry spell in early August, confirming our prior work that a reduction in water availability during summer can induce the end of cell production (Zhang et al. 2018). Given the evidence presented above and our prior experience with this system, the combination of a warm and dry early August likely anticipated growth termination of cell production in 2016. However, the growth resumption with a production of new earlywood-like cells occurred concurrently with the resumption occurrence of rather frequent and relatively large rainfall events. Therefore, the intense precipitation dynamics of mid-August under favorable warm temperatures very likely contributed to the IADF formation, at least for the trees that were vital enough to resume growth (Popkova et al. 2018).
Our findings indicate that the growth of our J. przewalskii was limited by a lack of cell turgor, even though cambial cell division and differentiation can require high levels of sucrose from photosynthesis (Deslauriers et al. 2016; Oribe et al. 2003). Drought can directly impact cambial activity earlier than indirectly via the reduction of photosynthesis under drought stress (Muller et al. 2011). This relationship mirrors Deslauriers et al. (2016), who found that cell division ceases when irrigation ceases. In fact, we found that the photosynthetic rate of J. przewalskii from 2011 to 2016 at our study site was higher during the end of cell production (Zhang 2018), supporting that newly assimilated carbon is not the main factor determining the cessation and resumption of wood production.
Our results support the hypothesis that the L-type IADFs observed in this study follow the similar mechanism described in trees living in the Mediterranean climate, i.e., that late growing season precipitation plays a crucial role for IADF formation (De Micco et al. 2016b). However, we cannot ignore the role of mild temperatures in the formation of IADFs in the cold Tibetan Plateau. Our investigations on these same trees show that radial growth can continue as long as the daily mean temperature remains above 6.1 °C and if there is sufficient precipitation (Zhang 2018). The warm conditions under which the resumption of rainfall occurred from mid-August through late September 2016, it is likely that tree water status was restored enough to resume cambial cell division and enlargement, as it can happen for the onset of xylogenesis in J. przewalskii has been described to be driven by an interaction of temperature and precipitation (Ren et al. 2018). Therefore, both the return of precipitation and the occurrence of warm conditions were vital for the resumption of new earlywood-like cells after the cessation in summer. In this case, the role of warm temperature on the L-type IADF formation in the annual ring is slightly different from the IADF formation in the Mediterranean region (Battipaglia et al. 2010b; Novak et al. 2013). These results highlight the great plasticity in growth response to extreme, transient meteorological events of this species.
4.2 Ecological implications of the IADF-related extended growing season
Our results showed that the majority of IADFs were formed in wider rings or observed in smaller trees, indicating that smaller trees or trees with wider rings were more sensitive to extreme meteorological events and thus more vigorous. These results also confirm previous observations of higher frequency of IADF in wider rings (Battipaglia et al. 2010a; Campelo et al. 2013) and, often, younger or smaller trees (Popkova et al. 2018; Rigling et al. 2001). Considering xylem cell production as an indicator of tree vigor, a higher xylem cell production could thus indicate higher growth resilience to unfavorable conditions and stronger capacity to resuming growth when the conditions return favorable. However, it is also possible that microsite conditions could also play an important role in regulating the resilience capacity. Microsite conditions at the dry, cool margin of growth have been shown to greatly affect the climatic response of trees (Bunn et al. 2005). Our observations support the call for continued integration of disciplines to understand the biotic and abiotic factors behind tree growth in extreme sites (Lloyd et al. 2017).
The occurrence of IADF in the dry and cold environment highlights the great phenological and growth plasticity of J. przewalskii to resiliently respond to short extreme events. Although future projections for the northeastern Tibetan Plateau indicate a trend towards a warmer, wetter climate, the seasonality of precipitation is uncertain (Gou et al. 2015) and events like the 2016 extreme drought could become more frequent. Based on our xylogenesis and additional documentation of frequent IADF formation across the larger tree population, we suspect that a substantial portion of the J. przewalskii on the northeast Tibetan Plateau might not simply stop cambial growth during a drought like that in 2016, but that a substantial proportion of trees are enough resilient to resume and extend growth if conditions return favorable.
The 1-month growth IADF-related extension in 2016 resulted in approximately 17% of additional annual stem biomass in the trees capable of resuming growth. Considering that 64% of all J. przewalskii trees in our study forest formed IADFs, the additional stem biomass production translates to a significant amount of carbon sequestered when compared to the less resilient non-IADF trees. Such additional growth could play an important role for forest carbon sequestration if such resilience is present in other species, at larger spatial scales, and other biomes.
Direct observations of cambial growth allowed us to identify the timing and the factors inducing IADF formation of J. przewalskii from a cool, arid, and continental region. Our observations indicated that precipitation during warm days in August and early September induced an additional month of growth in 64% of all trees that had stopped growing during the time of an extreme drought event. These findings both highlight the growth resilience of these trees and their flexibility to greatly extend the growing season when environmental conditions allow it. The response of trees to extreme, stressful, but transient meteorological events is one of the many uncertainties that require further study into how climatic change will impact forest ecosystems. Assessing tree species resilience to extreme event as performed in this study can provide important insight into mechanisms of growth responses that have implications for assessing forest carbon sequestration.
Most of the data used to support the findings of this study are included within the article; the rest are available from the corresponding author upon request.
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We thank Ming Lu, Haoge Niu, and Fang Wang for their kind field work. We also thank Drs. Ben Poulter and Ruben Manzanedo for their kind comments to improve the manuscript.
This work was funded by the China Postdoctoral Science Foundation (No. 2019M653788), the National Natural Science Foundation of China (Nos. 42001043 and 41771046), the Fundamental Research Funds for the Central Universities (No. lzujbky-2019-pd04), the 111 Project (No. BP2018001), and the National Science Foundation Macrosystem Biology program (EF-1241930).
Conflict of interest
The authors declare that they have no conflict of interest.
Statement on ethical approval
The authors declare that they obtained the approval of the Authority of Gansu Liancheng National Nature Reserve for conducting the study in Tulugou National Forest Park.
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Zhang, J., Alexander, M.R., Gou, X. et al. Extended xylogenesis and stem biomass production in Juniperus przewalskii Kom. during extreme late-season climatic events. Annals of Forest Science 77, 99 (2020). https://doi.org/10.1007/s13595-020-01008-1
- Climate change
- False rings