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Article

Xylogenesis Responses to a Mediterranean Climate in Holm Oak (Quercus ilex L.)

by
Iqra Liyaqat
1,
Angela Balzano
2,
Francesco Niccoli
1,
Jerzy Piotr Kabala
1,
Maks Merela
2 and
Giovanna Battipaglia
1,*
1
Department of Environmental, Biological and Pharmaceutical Sciences and Technologies, University of Campania Luigi Vanvitelli, 81100 Caserta, Italy
2
Department of Wood Science and Technology, Biotechnical Faculty, University of Ljubljana, 1000 Ljubljana, Slovenia
*
Author to whom correspondence should be addressed.
Forests 2024, 15(8), 1386; https://doi.org/10.3390/f15081386
Submission received: 11 July 2024 / Revised: 2 August 2024 / Accepted: 6 August 2024 / Published: 8 August 2024
(This article belongs to the Section Forest Ecology and Management)
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Abstract

:
Quercus ilex L., an evergreen oak species typical of the western and central Mediterranean basin, is facing decline and dieback episodes due to the increase in the severity and frequency of heat waves and drought events. Studying xylogenesis (the wood formation process) is crucial for understanding how trees respond with their secondary growth to environmental conditions and stress events. This study aimed to characterize the wood formation dynamics of Quercus ilex and their relationship with the meteorological conditions in an area experiencing prolonged drought periods. Cambial activity and xylem cell production were monitored during the 2019 and 2020 growing seasons in a Q. ilex forest located at the Vesuvius National Park (southern Italy). The results highlighted the significant roles of temperature and solar radiation in stimulating xylogenesis. Indeed, the correlation tests revealed that temperature and solar radiation positively influenced growth and cell development, while precipitation had an inhibitory effect on secondary wall formation. The earlier cell maturation in 2020 compared to 2019 underscored the impact of global warming trends. Overall, the trees studied demonstrated good health, growth and adaptability to local environmental fluctuations. This research provides novel insights into the intra-annual growth dynamics of this key Mediterranean species and its adaptation strategies to climatic variability, which will be crucial for forest management in the context of climate change.

1. Introduction

Climate change is exacerbating drought stress in Mediterranean ecosystems, negatively affecting plant growth, forest development and its ecosystem services [1]. Drought stress in trees is caused by a high evaporation rate, with concomitant low precipitation and high temperatures [2]; it mainly affects tree species that have a specific growing season or present strong adaptations to specific climatic conditions [3]. Despite being a drought-tolerant species widespread in the Mediterranean area, a decline in Quercus ilex L. has been reported in Southern Europe [4,5] at different locations inside its native distribution range due to climate changes [6], and its mortality rate might increase in future decades according to climatic projections [7]. Nevertheless, differences in microclimatic conditions, such as fluctuations in temperature, humidity, light intensity and soil moisture, can play an important role in the tree’s growth response [8,9,10]. Holm oak (Quercus ilex L.) grows and thrives better in regions with favorable microclimatic conditions characterized by sufficient soil moisture and moderate temperatures [11]. Conversely, harsh microclimatic conditions characterized by prolonged drought, extreme temperatures or poor soil conditions are detrimental to the health and growth of this tree species. Therefore, understanding the microclimatic variations within the holm oak’s habitat can provide insight into the health and resilience of this tree under different environmental conditions [12]. In addition, such an understanding can help in predicting the future spatial distribution of Q. ilex populations under changing climatic conditions [13]. Holm oak is an evergreen species widely spread in Mediterranean forests [14] and covers a large geographical range of the Mediterranean basin [15]. Species condense or extend their growth and reproduction seasons in adaptation to different environmental variables [16,17]. Certain oak species develop some physiological adjustments to deal with seasonal water scarcity [18,19]; particularly, during droughts in summer seasons, these evergreen species take advantage of underground water resources [20] or even adopt a bimodal growth pattern [21].
In dry tropical forests, xylogenesis is affected by seasonal variations and the severity of drought periods [22]. Drought periods force the cambium into a quiet or inactive state [23]. Along with seasonal boundaries, cambial activity is also controlled by the rate of cell production [24]. Previous studies have indicated that the growing season can be active until late summer if weather conditions are favorable for trees [25,26,27].
Trees growing in arid climates are the best candidates for detailed xylogenesis study due to the impact of seasonal water on tree growth [28,29]. To study the entire process of cambium cell activity and seasonal production, it is important to consider the effect of seasonal variability on xylem and phloem formation, as well as wood formation [30]. Additionally, secondary growth development as a response to environmental drought stress must be taken into consideration. Previous studies have shown that water stress also affects the vascular cambium [31,32], slowing cambial activity, shortening the cambial production period and producing small growth rings and intra-annual density fluctuations [33,34]. Understanding the impact of meteorological conditions on cambial activity is especially important for species which can adopt a bimodal growth pattern. This allows us to predict the amount of wood produced after summer and investigate their adaptative potential [35].
A recent study of the xylogenesis and phloem formation in Q. ilex trees at a particularly dry site in Naples revealed signs of distress. This is reflected in increased wood formation in autumn, and in some cases, the trees only form phloem and no xylem [36]. Dendrochronological studies in Vesuvius National Park showed a different growth response in Q. ilex according to the local site conditions, such as stand composition, stand density and slope and soil characteristics [11]. Recently, the drought response of different Mediterranean species at Vesuvius was studied by [37], showing Q. ilex to be susceptible to variations in precipitation, indicating that in the near future, this species could be severely affected by drought stress. Therefore, understanding the growth response of this species to microclimatic variations within its habitat can provide crucial insights into its health and resilience in different environmental conditions. It also underscores the importance of considering microclimate factors in assessing the overall well-being of tree species in their natural habitats.
In this study, we analyzed xylogenesis data on Q. ilex to study its cambial activity and cambial response in different seasons over two years in Vesuvius National Park, Southern Italy. The main goals were (a) to study the seasonal dynamics of xylogenesis (b), to assess the wood formation phases and (c) to understand the xylogenesis response to environmental stress in Mediterranean forests, especially drought. We hypothesized that Q. ilex species would present wood formation modifications according to climate fluctuations and drought stress.

2. Materials and Methods

2.1. The Study Area

The study site (Figure 1) is located within the Mediterranean region in Vesuvius National Park, which contains an active volcano with a long-documented history of eruptions. It is located in the eastern part of Naples (40°49′22.91″ N, 14°25′42.27″ E) along the Tyrrhenian coast of southern Italy. The Mediterranean forest is composed of mixed broadleaf forests, mixed coniferous vegetation and shrublands, and Quercus ilex L. is widespread in Vesuvius National Park [38,39].

2.2. The Sampling Microcores

Five healthy and vigorous trees of Quercus ilex were selected from a pure Quercus ilex stand (mean age of 80 ± 15; mean DBH of 40 ± 5.7; mean height of 21.4 ± 2.4). The trees belonged to a group of closely standing trees, and samples were taken from them every 2 weeks over the 2 years of monitoring (2019 and 2020). Microcores (1.8 mm in diameter) containing wood, cambium and bark were collected from the trunk at breast height by using the Trephor tool [27,40]. Each sample was extracted at 4–6 cm from the previous one in a spiral row around the trunk. The samples were immediately stored in F.A.A. (38% formaldehyde, glacial acetic acid, 50% ethanol—5/5/90 by volume) for one week; and after that, they were stored in 70% ethanol [41]. In total, we collected 200 samples, with 100 samples in 2019 and 100 samples in 2020.

2.3. Meteorological Data

The climate of the study area is Mediterranean, with rainy, mild winters and warm, dry summers [38]. The meteorological conditions of the reserve are monitored by a weather station, located 4.8 km from the examined forest plot (40°47′16.9″ N; 14°27′50.4″ E) and managed by the Campania Region. As we also wanted to evaluate the effect of incoming solar radiation, we downloaded the daily meteorological data of the ERA5-L and re-analysis [42]. The extraction of the data was performed in Google Earth Engine [43], where we extracted the values corresponding to the shape of the study area and the investigated time period (the years 2019 and 2020). Then, we tested the coherence of both datasets (see Supplementary Figure S1) for the common variables, which for temperature was excellent—R2 = 0.97 (p < 2 × 10−16) for maximum temperature, R2 = 0.98 (p < 2 × 10−16) for mean temperature and R2 = 0.94 (p < 2 × 10−16) for minimum temperature—and for precipitation was good, at R2 = 0.56 (p < 2 × 10−16), given that precipitation is a more localized phenomenon. The minimum, maximum and average daily temperatures and the daily total precipitation during the monitoring period (2019 and 2020) are shown in Figure 2.
The year 2019 was characterized by a consistent pattern of precipitation, peaking in November and showing drier conditions in the spring. In contrast, 2020 exhibited a pattern of more pronounced and extreme precipitation events, particularly evident as an unusually wet August. The driest period in 2019 occurred in June, while for 2020, this occurred in July. The year 2019 appears to have a higher likelihood of drought conditions, especially due to the specific mention of drier periods in the spring. In the subsequent analyses, we use daily total incoming radiation (MJ/day), the mean, minimum and maximum daily temperature (°C) and total precipitation (mm/day) from the ERA5 dataset.

2.4. Xylogenesis, Microscopy and Anatomical Criteria

To assess the tree growth response to environmental stress, we followed the xylogenesis process by observing the cambial activity and cell differentiation [36]. For this purpose, preserved samples were prepared using a paraffin-embedding technique and using a Leica TP1020 Automatic Benchtop Tissue Processor (Leica Biosystems Nussloch GmbH, Nußloch, Germany). Cross-sections of a 9 μm thickness were prepared by using Leica RM2245 - Semi Motorized Rotary Microtome (Leica Biosystems Nussloch GmbH, Nußloch, Germany). Finally, staining was carried out using a water solution containing 0.04% safranin and 0.15% astra blue (Sigma-Aldrich Chemie GmbH, Taufkirchen, Germany) [36], and permanent slides were prepared. The slides were examined under a Zeiss Axio Imager A.2 light microscope (Carl Zeiss Microscopy, White Plains, NY, USA). Images were taken at 20–100× using a Zeiss Axiocam 712 color camera (Carl Zeiss Microscopy GmbH, Jena, Germany). These images allowed us to study the cambial activity and the differentiation of xylem and phloem cells according to their cell wall thickness [44]. In detail, we measured cambial cells (CCs), which are identified by thin walls and small radial diameters. For each microcore, the cambial cells were counted in three radial directions, and then their average value was calculated [27,41]. Then, we focused on post-cambial cell (PCs), which are radially enlarged and not lignified, so their primary walls do not shine under polarized light as compared to other secondary wall-forming (SW) cells. In addition, we examined the mature cells (MCs), which are characterized by the total absence of protoplasts in the lumen and by fully thickened and lignified cell walls that shine under polarized light [45]. Finally, the non-collapsed phloem (NCP) was also analyzed, a portion of the phloem characterized by cells with intact cell walls and lumens, showing no signs of compression. For each microcore, the width of the cambial zone (in µm) containing the PCs, MCs and SW and NCP cells was measured.

2.5. The Rolling Window Correlation Analysis

To understand the influence of the meteorological conditions on xylogenesis, Pearson’s correlations tests between the xylogenesis variables and the previous weather conditions were conducted [17]. The meteorological data were aggregated over time windows varying in length between 1 and 60 days before each sampling date, and the minimum, maximum and mean temperature, mean radiation and sum of precipitation were computed for each of these time intervals. Then, for each window length, Pearson’s correlation between the CC count, PC, SW and MT width and the meteorological parameters was computed using the Hmisc package in Rstudio (Version 4.4.1), with a significance threshold of p < 0.05. This procedure allowed us to evaluate the length and timing of the time intervals during which the meteorological conditions influence the different wood formation stages. In parallel, the same analyses were performed with the meteorological data of the weather station to ensure that the results obtained with the gridded dataset were consistent with the local observations. These results are reported in the Supplementary Materials (see Figure S2).

3. Results

3.1. Cambial Activity and Xylem Formation

The numbers of CCs for 2019 and 2020 show different patterns of cambial activity (Figure 3). For both years, the CCs have the minimum values at the beginning of April (Day of the year, DOY 91–92) and start to increase at the end of April.
In 2019, the number of CCs at the beginning of the year was just over four cells and showed only slight fluctuations in the following months. The highest peak in the CC count was recorded around the end of May (DOY 150), when the count was just over six cells. This period precedes the summer temperature peak and coincides with moderate precipitation, possibly creating a favorable environment for cambial activity. Despite this slight increase, the CC counts remained relatively stable in the range of four to six cells per square millimeter for the duration of the year. In contrast, in 2020, the CCs were characterized by greater variability in numbers. The highest peak occurred around the beginning of September (DOY 250), when the CC counts approached eight cells, a significant increase compared to the previous year’s peak. This notable increase in cambial activity followed the highest summer temperatures observed in August, concurrent with an increase in precipitation, which may have synergistically contributed to the growing conditions. After this peak, the CC numbers declined but remained slightly above the range documented for 2019 for the remainder of the year. While the beginning of both years was characterized by similar CC numbers, the substantial peak seen in 2020 was not observed in 2019, indicating a period of increased cambial activity or growth in the later part of 2020.
In both years, there was a slight increase in CCs in December. December in both years was one of the wettest months, and in both years, the average temperature was still over 10 degrees. Likely, the moisture availability and the mild temperature could have enhanced the cambial activity at this time. The presence of PCs (post-cambial cells) indicated that the cambium was still active in this time period, producing new xylem cells. In the year 2019, from the beginning of the sampling period, no PCs were observed, but they started to appear at the end of April (DOY 120), while in 2020, we observed the production of a few PCs in the middle of April (DOY 106 and 119) (Figure 3). The number of PCs started to increase in the middle of May in 2019 (DOY 134). In this period, less precipitation was recorded in 2019 as compared to 2020. In the middle of the year, in the spring season, the pattern for the formation of PCs was similar for both years. In both years, the highest number of PCs was measured in the month of June, and this time period was recorded as the warmest in both years. The PC number started to decline in mid-August (DOY 230) in both years. At the end of September (DOY 254–257), in both years, a new increase in the number of PCs was noticed, and in this time period, the precipitation level was high and the temperature still mild.
The SW (secondary wall) cell formation time period in the years 2019 and 2020 was slightly different (Figure 3). In the year 2019, SW cell formation was noticed at the end of April (DOY 120) and showed its peak in the beginning of July (DOY 188), the warmest period, which could represent the start of latewood. Meanwhile, in 2020, for the first two months of sampling, March and April, no formation of new rings was observed. Newly formed cell production was observed in the middle of May (DOY 134), and it remained for more or less the whole year. The peak for this year was observed at the beginning of July (DOY 191), and this was the driest time period for 2020. In both years, we also observed a low number of SW cells in the month of December (DOY 357).
MT (mature cell) formation was not observed in the first few months of the sampling period in both years, but after that, it continued until the end of the year (Figure 3). In 2019, the cell maturation phase started in mid-May and continued until the end of the year. However, in 2020, cell maturation started at the beginning of June (DOY 161), and it continued until full cell maturation. The final value for the MTs was higher for the year 2020 than for 2019, as also reflected in the final wood produced and tree ring width (Figure 4), suggesting that the climatic conditions in the year 2020 were more favorable for wood formation that those that occurred in 2019.
The non-collapsed phloem (NCP) (Figure 5) pattern indicates more variability in 2020 than in 2019. The presence of non-collapsed phloem (NCP) was noticed on all DOY in both 2019 and 2020. We found the maximum width of the NCP at DOY 120 and then at 274 for the year 2019. We also observed a similar increment in the width of the NCP at the end of the sampling period in 2019. For the year 2020, the maximum area for the NCP was measured at the start and at the end of the year (DOY 119 and 329). As compared to 2019, at the end of the sampling year in 2020, the minimum width of the NCP was observed. In both years, the maximum width of the NCP occurred in the month of April during the spring season.

3.2. Rolling Window Results

From the rolling window correlation analysis, no significant correlations emerged for the CC count. The PC width was positively correlated with the minimum, mean and maximum temperatures for time windows of 10 days or fewer before the sampling, and incoming radiation was correlated with PC width for all the window lengths considered (Figure 6). On the other hand, there were some sporadic negative correlations with precipitation. The SW cell width was significantly positively correlated with the mean and maximum temperatures for all the window lengths considered and with the minimum temperatures between 1 and 50 days before; however, the strength of the correlation decreased with an increase in the window length. A positive and strong correlation between SW cells and radiation was present for all the windows lengths considered, while on the other hand, the correlation between SW cells and precipitation was significant and negative for window lengths between 5 and 60 days. Finally, the MT width only showed a significant correlation with temperature for longer window lengths. These results are coherent with what emerged from the meteorological data recorded by the weather station (Supplementary Figure S2).

4. Discussion

In the context of climate change, Quercus ilex L. faces increased risks of dieback, particularly in Mediterranean regions. Research indicates that prolonged drought, combined with high temperatures and pathogen attacks, contributes significantly to this phenomenon [46,47]. Dieback is often characterized by a reduction in canopy density, yellowing of the leaves and the progressive death of branches and eventually entire trees [47]. This decline is particularly worrying as besides affecting individual trees, it disrupts ecosystem functions and forest biodiversity.
Understanding the growth patterns and resilience of Quercus ilex in our study helped us illuminate how these trees might respond to the increasing frequency and severity of drought conditions under climate change.
The results of this study showed how xylogenesis in Quercus ilex, a widespread Mediterranean species, was significantly influenced by temperature and solar radiation. These factors are crucial for optimizing the growth and acclimatation mechanisms of this species to the Mediterranean climate, which is characterized by abundant solar irradiance and high temperatures during the growing season.
In 2019, the peak in cambial cells (CCs) at the end of May aligned with the onset of warmer temperatures and sufficient rainfall, indicating a supportive climate for the tree’s developmental processes. In contrast, in 2020, the CCs showed a significant increase in early September. This resumption of growth, following August rainfall events that replenished the soil moisture levels, along with persisting high temperatures, highlights the dynamic environmental response of the trees to changing weather conditions. The holm oak trees took advantage of the conditions that promoted growth irrespective of the timing of their occurrence during the year, as already reported for other species in Mediterranean environments [26,35,48,49].
After a drought, sudden increases in rainfall and continued high temperatures might have promoted growth processes to take advantage of those conditions.
In the Quercus ilex growing at a site in Naples during an extremely dry year, a remarkable increase in cambial activity and wood formation was found in autumn with the formation of intra-annual density fluctuations (IADFs) [36]. The growth increment occurring in autumn was greater than that in spring; moreover, in some cases, only phloem—but not xylem—was formed (as proved by the lack of PCs or SW cells during the sampling year), suggesting that these trees experienced high stress [36]. IADFs are characteristic features in tree rings; they represent variations in wood density that occur within a single growing season [50]. These fluctuations are often an indication of the tree’s physiological response to changing environmental conditions, particularly in relation to water availability and temperature [21,34,50,51]. In Mediterranean climates, IADFs in Quercus ilex have primarily been associated with variations in water stress and temperature fluctuations. The presence of IADFs may indicate periods of drought stress followed by recovery or sudden changes in moisture availability [51,52,53,54].
IADFs in Q. ilex occurred more frequently in years with pronounced drought followed by intense rainfall, reflecting the tree’s adaptation to an unpredictable water supply [55,56]. The formation of IADFs can therefore be seen as an adaptive strategy that allows Q. ilex to modulate its growth in response to intra-annual climate variability, especially under the challenging conditions of the Mediterranean environment.
The absence of IADFs in the trees we analyzed suggested less pronounced fluctuations in water availability or a more stable growing environment at our site for Q. ilex compared to the conditions that occurred at the site in Naples. The trees in the current study have a less extreme climate, which allows them to maintain regular growth cycles.
However, the research by [11] in Vesuvius National Park showed that local site factors such as the stand composition, density, and slope and soil characteristics could have a significant impact on the growth response of Q. ilex. This diversity demonstrated the ecological plasticity of the species, meaning that certain populations may show signs of fragility in certain microclimatic situations, while other populations may demonstrate resilience and adaptability.
There was a clear correlation between temperature and the formation of new xylem cells, as shown by the timing and peaks of post-cambial cell (PC) and secondary wall (SW) cell formation. This pattern was consistent with the results of [57,58], which showed that the two main factors influencing cambial activity and wood development in Mediterranean tree species were temperature and precipitation.
Precipitation had a more complicated and often inhibitory influence, while temperature and solar radiation appeared to be the main positive factors. These discoveries added to our knowledge of how Q. ilex is able to acclimate to its Mediterranean habitat by striking a balance between optimizing development and responding to changing moisture levels. The results of the rolling window correlation study showed a positive correlation (r Pearson’s correlation ranking around 0.25 and 0.50) between PC width and temperature and incident radiation, suggesting that these variables were crucial in the initial stages of xylem formation. High temperature may determine the early xylem development rate [59], supporting a positive relationship between PC width and temperature.
The growth of secondary wall cells may be favored by drier conditions, as shown by the clear positive correlation between SW cell width and temperature and its negative correlation with precipitation.
Precipitation, on the other hand, had a more complex and often inhibiting effect (r Pearson’s correlation = −0.25), especially when it came to the growth of secondary wall cells, where dry conditions seemed to be more favorable. Moreover, precipitation is negatively associated with radiation availability, which is one of the most important drivers of photosynthesis [60,61,62], and we found strong positive correlations between radiation and the different stages of xylogenesis.
We found differences in the timing of SW cell development between the two years. In 2019, during the warmest part of the year, it began in late April and peaked in early July. In 2020, on the other hand, this process started in mid-May, continued throughout the year and peaked in early July. This means that the timing and speed of SW cell production were significantly influenced by external factors, especially temperature. The negative correlation between SW cell width and precipitation [63] suggested that lower moisture could promote the formation of secondary walls, possibly as an adaptation strategy to drought. The earlier onset of mature cell (MT) formation in 2020 compared to 2019 suggested that warming trends, as noted by [36], can accelerate the maturation phase in Q. ilex.
The correlations with the meteorological data indicated that although the trees adapted to the temperature and precipitation fluctuations, they showed no signs of severe stress or dysfunction. This emphasized the crucial influence of climate, especially rainfall and moisture availability, on the health and stress levels of these trees. However, the fluctuations between 2019 and 2020 also underlined the importance of long-term monitoring to understand the impact of climate variability on forest dynamics and the adaptation strategies of trees such as Quercus ilex in Mediterranean ecosystems. The variability of CCs and PCs observed in this study mirrored the significant year-to-year variability in growth responses due to fluctuating climatic conditions in other Mediterranean tree species [54].
Non-collapsed phloem (NCP) showed peaks in width in spring, indicating that early favorable conditions significantly influence phloem production. These observations were consistent with previous studies that found that phloem production is maximized in Mediterranean trees in response to favorable conditions early in the year [44,64]. The NCP was less affected by environmental conditions, and more xylem than phloem was produced, as is the case for trees growing in favorable conditions [64].
Overall, 2020 appeared to be more favorable for Quercus ilex wood formation than 2019, which experienced more drought conditions, as eventually reflected in the greater final annual ring width.
The results of the current study showed that Quercus ilex can acclimate to fluctuations in temperature and precipitation without severe stress or dysfunction. However, it is important to take in account that the deposition of cell layers and the formation of xylem and phloem are determined not only directly by environmental conditions but also by many other endogenous processes, such as photosynthesis, the translocation of photosynthates and plant water status [65], which are, in turn, sensitive to climatic conditions [66].
Overall, these results deepen our understanding of how this tree species responded to environmental conditions, as well as the crucial influence of climate on holm oak health and stress levels. This is crucial for developing strategies to mitigate the impacts of the dieback of this important species and ensure the conservation of Mediterranean oak forests.

5. Conclusions

This study provided a thorough investigation of the growth processes of Quercus ilex L. for two years under different environmental conditions. The results showed the crucial role that temperature and solar radiation play in stimulating xylogenesis, allowing these trees to reach their full growth potential in a Mediterranean climate. The trees in this study showed healthy growth and no dysfunction, indicating their adaptation to local environmental fluctuations.
Our understanding of the different effects of temperature, solar radiation and precipitation on the different stages of wood formation was improved by the correlation analysis of the rolling windows. The differential response of Mediterranean species to their specific climatic conditions was highlighted by the positive correlation of growth with temperature and solar radiation and the development of post-cambial and secondary wall cells, as well as the inhibitory effect of precipitation on secondary walls. The fact that the cells matured earlier in 2020 than in 2019 confirmed the plasticity of Quercus ilex and its ability to respond to different environmental conditions.
Overall, this study emphasized the importance of long-term monitoring to fully understand how climate variability will affect forest dynamics and how Mediterranean trees, such as Quercus ilex, a widespread species but for which there is limited available information, will adapt. The knowledge gained here contributes to our understanding of how these trees optimized their growth, balancing adaptations to fluctuating moisture levels and the overall effects of climate on their well-being and stress responses.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/f15081386/s1. Figure S1. Comparison of the weather station against ERA-5 daily meteorological data for the common variables: (a) maximum temperature, (b) mean temperature, (c) minimum temperature and (d) total precipitation; Figure S2. Rolling windows correlations between xylogenesis variables and ground meteorological station data. CC = cambial cells (number of cells), PC = post-cambial cells (width, μm), SW = secondary wall-forming cells (width, μm), MT = mature cells (width, μm). Meteorological variables: mean temperature (°C), maximum temperature (°C), minimum temperature (°C), mean radiation (MJ/day), and total precipitation (mm/day). Positive correlations are displayed in red, negative correlations in blue, non-significant ones in grey.

Author Contributions

Conceptualization, G.B.; methodology and software: I.L. and J.P.K.; investigation, I.L., A.B., F.N., J.P.K., M.M. and G.B.; resources, G.B.; writing—original draft preparation, I.L. and A.B.; writing—review and editing, I.L., A.B., F.N., J.P.K., M.M. and G.B.; supervision, A.B. and G.B. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Data Availability Statement

The data presented in this study are available on request from the corresponding author.

Acknowledgments

This research is linked to activities conducted within the MIUR Project (PRIN 2020) “Unravelling interactions between WATER and carbon cycles during drought and their impact on water resources and forest and grassland ecosySTEMs in the Mediterranean climate (WATERSTEM)” (protocol code: 20202WF53Z). In addition, this research is supported by the Program P4 0015 of the Slovenian Research Agency. Finally, the authors would like to thank Katerina Čufar for her invaluable advice.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Study site located within Vesuvius National Park, Naples. Red triangle indicates the Quercus ilex stand.
Figure 1. Study site located within Vesuvius National Park, Naples. Red triangle indicates the Quercus ilex stand.
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Figure 2. Weather conditions of the study site during the monitoring period of 2019 and 2020. In red, the maximum temperature; in black, the average temperature; in grey, the minimum temperature. The blue bars represent precipitation.
Figure 2. Weather conditions of the study site during the monitoring period of 2019 and 2020. In red, the maximum temperature; in black, the average temperature; in grey, the minimum temperature. The blue bars represent precipitation.
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Figure 3. Number of cambial cells and width of different developmental xylem zones in Quercus ilex trees in 2019 (A–D) and 2020 (E–H): cambial cells (CCs), enlarging post-cambial cells (PCs), cells developing secondary walls (SW) cells and mature (MT) cells with a lignified secondary wall. Mean values are shown for the days of the year (DOY) when the sampling was performed.
Figure 3. Number of cambial cells and width of different developmental xylem zones in Quercus ilex trees in 2019 (A–D) and 2020 (E–H): cambial cells (CCs), enlarging post-cambial cells (PCs), cells developing secondary walls (SW) cells and mature (MT) cells with a lignified secondary wall. Mean values are shown for the days of the year (DOY) when the sampling was performed.
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Figure 4. Final tree ring width (TRW) containing fully mature cells formed for the years 2019 and 2020. Scale bar = 200 µm.
Figure 4. Final tree ring width (TRW) containing fully mature cells formed for the years 2019 and 2020. Scale bar = 200 µm.
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Figure 5. Non-collapsed phloem (NCP) width in 2019 (A) and 2020 (B). Mean values are shown on the days of the year (DOY) when the sampling was performed.
Figure 5. Non-collapsed phloem (NCP) width in 2019 (A) and 2020 (B). Mean values are shown on the days of the year (DOY) when the sampling was performed.
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Figure 6. Correlations between xylogenesis and meteorological conditions. CC = cambial cells (number of cells), PC = post-cambial cells (width, μm), SW = secondary wall-forming cells (width, μm), MT = mature cells (width, μm). Meteorological variables: mean radiation (MJ/day), maximum temperature (°C), mean temperature (°C), minimum temperature (°C), and total precipitation (mm/day). Positive correlations are displayed in red, negative correlations in blue, non-significant ones in grey.
Figure 6. Correlations between xylogenesis and meteorological conditions. CC = cambial cells (number of cells), PC = post-cambial cells (width, μm), SW = secondary wall-forming cells (width, μm), MT = mature cells (width, μm). Meteorological variables: mean radiation (MJ/day), maximum temperature (°C), mean temperature (°C), minimum temperature (°C), and total precipitation (mm/day). Positive correlations are displayed in red, negative correlations in blue, non-significant ones in grey.
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MDPI and ACS Style

Liyaqat, I.; Balzano, A.; Niccoli, F.; Kabala, J.P.; Merela, M.; Battipaglia, G. Xylogenesis Responses to a Mediterranean Climate in Holm Oak (Quercus ilex L.). Forests 2024, 15, 1386. https://doi.org/10.3390/f15081386

AMA Style

Liyaqat I, Balzano A, Niccoli F, Kabala JP, Merela M, Battipaglia G. Xylogenesis Responses to a Mediterranean Climate in Holm Oak (Quercus ilex L.). Forests. 2024; 15(8):1386. https://doi.org/10.3390/f15081386

Chicago/Turabian Style

Liyaqat, Iqra, Angela Balzano, Francesco Niccoli, Jerzy Piotr Kabala, Maks Merela, and Giovanna Battipaglia. 2024. "Xylogenesis Responses to a Mediterranean Climate in Holm Oak (Quercus ilex L.)" Forests 15, no. 8: 1386. https://doi.org/10.3390/f15081386

APA Style

Liyaqat, I., Balzano, A., Niccoli, F., Kabala, J. P., Merela, M., & Battipaglia, G. (2024). Xylogenesis Responses to a Mediterranean Climate in Holm Oak (Quercus ilex L.). Forests, 15(8), 1386. https://doi.org/10.3390/f15081386

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