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Article

Comparison of C, N and P Stoichiometry in Different Organs of Fraxinus velutina

by
Linshui Dong
1,
Aiyun Song
1,*,
Jianfeng Zhang
2,
Ling Peng
1,
Nannan Cheng
3 and
Banghua Cao
4
1
Shandong Provincial Key Laboratory of Eco-Environmental Science for Yellow River Delta, Binzhou University, Binzhou 256600, China
2
Institute of Subtropical Forestry, Chinese Academy of Forestry, Hangzhou 311400, China
3
School of Forestry and Wildlife Sciences, Auburn University, Auburn, AL 36949, USA
4
Key Laboratory of State Forestry Administration for Silviculture of the Lower Yellow River, Shandong Agricultural University, Taian 271018, China
*
Author to whom correspondence should be addressed.
Forests 2023, 14(1), 64; https://doi.org/10.3390/f14010064
Submission received: 24 November 2022 / Revised: 23 December 2022 / Accepted: 26 December 2022 / Published: 29 December 2022
(This article belongs to the Topic Urban Forestry and Sustainable Environments)
Browse Figures
Versions Notes

Abstract

:
Velvet ash (Fraxinus velutina Torr.) is a dioecious tree species, which is widely used as a part of urban greeneries in saline land of North China. Female and male trees have different nutrient allocation trade-offs in dioecious species. As the fruit production consumes a lot of nutrients, female F. velutina plants grow slowly and are vulnerable to insects and diseases. Ecological stoichiometry can be used to study the physiological mechanism of the growth difference between female and male plants. The purpose of this study was to compare the seasonal patterns of C, N and P stoichiometry and their trade-offs in different organs of female and male F. velutina plants planted in urban green spaces. The fruit C, N and P contents of female F. velutina plants were all lower than those of leaves in the early growing season, but higher than those of leaves in the middle and late growing season. During most months, the leaf C and P contents of females were higher than those of males, while the leaf N content was lower than that of males, which was consistent with the sex-specific resource requirements for reproduction (i.e., high carbon requirements for ovules and high nitrogen demands for pollen). Compared to the females, there were more significant correlations between the stoichiometric indices (element contents and their ratios) of branches and leaves in male plants, and this difference may be related to the fact that the male plants were not involved in nutritional allocation for fruits. The leaf N/P of F. velutina was lower than 14 in the whole growing season, which indicated N limitation. The female and male plants of F. velutina had different sex-specific resource requirements for sex organ formation.

1. Introduction

Ecological stoichiometry studies the balance of multiple chemical elements in ecological interactions. Plants stoichiometry predicts the relationship between element contents and growth rate and studies resource allocation strategies between the different organs of plants [1,2]. The different nutritional element concentrations in plant organs reflect nutrient uptake and utilization efficiency during plant growth [3]. The carbon, nitrogen and phosphorus contents of plant organs are known to be common functional traits, which are studied progressively as a basic framework to comprehend survival strategies adopted by plants for the acquisition and investment of resources [4,5].
Dioecious species have to satisfy gender reproductive demands; female plants have higher reproductive efforts, causing different nutrients allocation trade-offs [6,7,8]. In recent years, many studies have used plant stoichiometry in studying C (carbon), N (nitrogen) and P (phosphorus) [9,10,11], but there are few studies concerning the resource allocation strategies of female and male plants based on stoichiometry. The leaf N and P contents in male plants of Cercidiphyllum japonicum Sieb. et Zucc. were higher than those of female plants, but the leaf C/N and C/P of male plants were lower than those of female plants [12]. The needles of Juniperus communis L. females had higher N concentration in March and April, and this dropped to the same level as males after flowering and vegetative growth began. On the other hand, in Taxus baccata L., N concentration was higher in males throughout the growing season, but the highest differences appeared in intensive shoot elongation and radial growth [13]. Recent studies have found that the twigs of female plants of Acer pensylvanicum L. have higher nonstructural carbohydrates concentrations than that of male plants [14].
Velvet ash (Fraxinus velutina), a non-native dioecious species introduced from the United States, is widely used as a part of urban greeneries in saline land of North China, as it displays excellent salt resistance [15,16]. The female F. velutina plants grow slowly and are vulnerable to insects and diseases due to the large amount of nutrients consumed by fruit production, and the differences in height and the diameter at breast height (DBH) between female and male plants become increasingly obvious as the plants grow [17]. Understanding the physiological mechanism of the growth difference between female and male plants can provide a theoretical basis for formulating reasonable stand management measures. However, the physiological mechanism of the growth difference between the female and male plants of F. velutina has not been comprehensively studied. Ecological stoichiometry is an effective method to study the difference in nutrient resources allocation strategies between the plants.
In this study, we compared the stoichiometric characteristics of different organs of the female and male plants of F. velutina and analyzed the nutrient allocation trade-off strategies among their different organs. This study aimed: (i) to compare the seasonal patterns of carbon, nitrogen and phosphorus stoichiometry in different organs of female and male F. velutina plants, (ii) to analyze the correlation between the stoichiometric indices of different organs of F. velutina, and (iii) to assess whether F. velutina in the study area is mainly limited by nitrogen or phosphorus. The findings of this research can provide a theoretical basis for further revealing the physiological mechanism of growth differences between the female and male plants of F. velutina.

2. Materials and Methods

2.1. Study Site

Located in the Yellow River Delta and Bohai Sea coastal region, Binzhou city of Shandong Province of China belongs to a coastal alluvium plain with an average altitude of 12 m. Binzhou city has a temperate continental monsoon climate with cold and dry winters. The annual average temperature is 12.7 °C, ranging from 39.5 °C in summer to −18.4 °C in winter. The average annual precipitation is 560 mm, with nearly 70% of the precipitation falling between May and September. The investigated plantation of F. velutina was located in urban public green spaces of Binzhou City in Shandong Province of North China (37°23′ N, 118°01′ E). The soil is slightly saline in this plantation, and the soil properties are shown in Table 1, which shows the average values of soil indices from six random soil samples at the experimental site.

2.2. Experimental Design and Sample Collection

A plot of 20 × 40 m2 in the F. velutina plantation was established in 2016, and we collected the data during the growing season (May to November). The total number of trees is 153, including 67 females and 86 males, and they were planted 21 years ago with seedlings that were purchased from Shandong Huaxiang Forest Seedling Co., Ltd. The average height of all the trees in the above plot is 11.59 m and the average diameter at breast height (DBH) is 17.08 cm. The average height of all female trees in the plot is 10.61 m, and their average DBH is 15.84 cm. The average height of all male trees in the plot is 12.37 m, and their average DBH is 17.98 cm. According to the height (>9.5 m) and DBH (17.08 ± 2 cm), we randomly selected twenty-four healthy F. velutina with twelve female trees and twelve male trees as our marked sample trees. In the middle of each month from May to November, we took samples, including leaves, fruits, and branches (biennial), from female trees, and leaves and branches (biennial) from male trees. In November, only fresh leaves were collected because of sample consistency. We took samples in four directions (north, south, east, and west) from the center of the crown of each tree. Each type of sample (leaves, fruits, or branches) from four directions was mixed as a combined sample in equal portions for a chemical test.
The plant samples were washed and dried at 105 °C for 30 min, and then dried at 75 °C to obtain a constant weight. Then, they were ground and passed through a 60-mesh sieve. The total C and N contents of the plant samples were measured by using an element analyzer (Vario EL III, Elementar Inc., Langenselbold, Germany). The total P of the plant samples was measured using the HClO4–H2SO4 colorimetric method [18,19].

2.3. Data Analysis

All tests were conducted using SPSS 19.0 and R (version 4.0.1), and statistical significance was determined when p < 0.05. In each month of the growing season, the C, N and P contents and their ratios in different organs of the female and male plants were calculated separately. The statistical methods of a one-way ANOVA (analysis of variance) and LSD multiple comparisons (least significant difference test) were used [20]. Letter display was used in multiple comparisons, and the same stoichiometric indices of different months not sharing the same letter indicated significant differences at an alpha level of 0.05, according to an LSD test. Pearson’s correlation coefficient in R with the psych package was used to measure the linear association between the stoichiometric indices of different organs of F. velutina. It should be noted that the data used for the correlation analysis in Table 2 and Table 3 include the element content data of different organs of plants in the middle growth stages (July, August, and September).

3. Results

3.1. Dynamics of C, N and P Contents in Different Organs of Female Plants of F. velutina

The C, N and P contents of the leaf, fruit and branch of female F. velutina were compared in the growing season (Figure 1). The range of leaf C content was 444–468.38 g kg−1 during the growing season, while fruit C was 462.06–491.89 g kg−1, and branch C was 422.15–464.65 g kg−1. The C contents of leaf and branch in the late growing season were lower than those in the early and middle growing season. The fruit C content of female plants showed a gradual increasing trend during the growing season. The C content of fruit was greater than that of leaf and branch, especially in the middle and late growing season.
The ranges of N content in the leaf, branch and fruit of female F. velutina were 9.79–26.78 g kg−1, 4.08–6.84 g kg−1 and 10.33–22.53 g kg−1, respectively. The ranges of P content in leaf, branch and fruit were 1.37–2.79 g kg−1, 0.70–0.91 g kg−1, and 2.00–3.18 g kg−1, respectively. During the growing season, the N and P contents of leaf gradually decreased, while the N and P contents of fruit gradually increased. The branch N content gradually increased during the whole growing season, while the branch P content was relatively stable.
The contents of N and P in branch were significantly lower than those of leaf and fruit during the growing season. The N content of leaf from May to August was higher than that of fruit, but it was lower than that of fruit in the late growing season. The P content of leaf in the early growing season (May to June) was higher than that of fruit, but it was lower than that of fruit in the later growing period. The N and P contents of fruits were higher than that of leaves in the late growing season, which was related to nutrient resorption.

3.2. Dynamics of C, N and P Contents in Different Organs of Male Plants of F. velutina

The leaf C content of male plants varied from 434.49 to 460.00 g kg−1, and the branch C content ranged from 439.28 to 464.67 g kg−1 (Figure 2a). The leaf C and branch C content of male plants showed a general downward trend throughout the growing season. During the growing season, the content range of the leaf N of male plants was 9.63–25.94 g kg−1, branch N was 3.83–7.86 g kg−1, and the leaf P content of plants varied from 1.38 to 2.65 g kg−1, while the branch P content varied from 0.71 to 1.06 g kg−1 (Figure 2b,c). The leaf N and leaf P contents of male plants gradually decreased during the growing season, the branch N contents gradually increased throughout this period, while the branch P contents remained relatively stable from June to November.
The leaf C and branch C contents of male plants were relatively similar in each month of the growing season. The leaf N and leaf P contents of male plants of F. velutina were both higher than those of the branch in each month of the growing season. In May, the N and P contents of leaves were 6.64 times and 3.73 times higher than those in branches, respectively, but in November, the difference of the N and P contents between them became relatively small.

3.3. Dynamics of C/N/P Ratios in Different Organs of Female Plants of F. velutina

The leaf C/N ratios of female plants varied from 17.51 to 51.02, those of branch varied from 64.03 to 116.55, and those of fruits varied from 22.39 to 44.73 during the growing season (Figure 3a). The leaf C/P ratios varied from 171.04 to 304.45, those of branch varied from 477.18 to 670.32, and those of fruit ranged from 152.58 to 234.48 (Figure 3b). The branch C/N and C/P ratios of female plants in each month were significantly greater than those of leaf and fruit. The fruit C/N and C/P ratios in the first half of the growing season were mostly larger than those of leaf, while the fruit C/N and C/P ratios in the second half of the growing season were mostly smaller than those of leaf.
In the growing season, both the C/N and C/P ratios of the branch or fruit of female plants showed a downward trend, especially after September. The leaf C/N ratios of female plants showed a gradual upward trend in the growing season, while the leaf C/P ratios remained stable, except in November. The leaf C/N and C/P ratios in November were significantly greater than those in other months. The monthly change trends of the C/N and C/P ratios in different organs were opposite to those of the N contents and P contents, respectively, which showed that the variation in the two ratios were mainly determined by the N and P contents (Figure 1 and Figure 3).
The leaf N/P of female plants ranged from 6.60 to 11.62, the branch N/P varied from 5.80 to 8.01, and the fruit N/P varied from 5.41 to 7.12 (Figure 3c). The N/P ratios of branch and fruit gradually increased during the growing season, while the N/P ratio of leaf gradually decreased during this period. In each month of the growing season, the N/P ratios of fruit and branch were all relatively similar. The leaf N/P of female plants was significantly greater than that of branch and fruit in the early and middle growing season, while the leaf N/P was close to that of branch and fruit in the late growing season.

3.4. Dynamics of C/N/P Ratios in Different Organs of Male Plants of F. velutina

The leaf C/N ratios of the male plants of F. velutina ranged from 18.18 to 48.87, and the branch C/N ratios varied from 58.85 to 126.72 (Figure 4a). The range of the leaf C/P ratios of male plants was 177.40–376.12 (Figure 4b), while the range of the branch C/P ratios of male plants was 399.43–708.90. The branch C/N and C/P ratios of male plants in each month were significantly greater than those of leaf. Both the C/N and C/P ratios of branch showed a decreasing trend in the growing season. Except at the end of the growing season, there was no significant difference between leaf C/N ratios in different months, and the same was true for leaf C/P ratios.
The leaf N/P of male plants varied from 8.03 to 11.60 in the growing season, and the branch N/P of male plants varied from 5.81 to 7.91 (Figure 4c). Except for November, the leaf N/P of male plants was significantly greater than that of branch in other months. The branch N/P ratios gradually increased from May to November, but there was no significant difference in branch N/P ratios between months from May to October. From May to November, the leaf N/P showed a trend of increasing first and then decreasing. Except for November, the difference between leaf N/P ratios in different months did not reach a significant level. Similar to female plants, the ratios of N/P in the branch and leaf of male plants were also relatively close at the end of the growing season in November.

3.5. Gender-Related Differences in C, N and P Contents and Their Ratios in the Leaf and Branch of F. velutina

The C, N and P contents in the leaf and branch of female and male plants were compared (Figure 5 and Figure 6). The leaf C and P contents of female F. velutina were both higher than those of male plants in most growth stages, but the gender-related differences were not significant in each month (p < 0.05). However, the leaf N content of female plants was lower than that of male plants in most months, but the difference was significant only in October (p < 0.05). There were no significant differences in branch C and P contents between female and male F. velutina in each month (Figure 6). However, the branch P content of female plants was lower than that of male plants in each month of the growing season. The branch N content of female plants was lower than that of male plants from June to November, while the differences in branch N contents between the female and male plants were all significant in each month from July to November (p < 0.05).
The leaf C/N ratio of females was slightly higher than that of male plants in most months, and the leaf N/P ratio was lower in females than in males in most months (Figure 7). The branch C/N ratio of female plants was higher than that of male plants in most months of the growing season (Figure 8), and the sexual differences were significant in July, September and October (p < 0.05). The branch C/P ratios of female plants were slightly higher than those of male plants, and the difference was significant in October (p < 0.05). There were no significant differences in branch N/P between the female and male plants of F. velutina in each month of the growing season.

3.6. Correlation of C, N, P and Their Ratios in Different Organs of Female F. velutina in the Middle of the Growing Season

The relationship between C, N and P contents and their ratios in the leaf, branch and fruit of female plants in the middle of the growing season (i.e., July, August and September) was analyzed using Pearson’s correlation coefficient (Table 2). The correlation analysis of C, N and P contents in the same organ of female plants showed that only leaf C and leaf N, fruit N and fruit P had a significant correlation (p < 0.05).
In the same organ (leaf, branch or fruit), the C/N and C/P ratios had a highly significant negative correlation with the corresponding N and P content, respectively (p < 0.01), but most of which had no significant correlation with the corresponding C content. This showed that the variation in the C/N and C/P ratios of leaf, branch and fruit was mainly determined by their N or P contents. Most N/P ratios had highly significant correlation with their corresponding N or P content of the same organ (p < 0.01), but branch N and branch N/P had no significant correlation, and fruit P had no significant correlation with fruit N/P.
The correlation between the three element contents of different organs was analyzed. Leaf N had a highly significant negative correlation with fruit N content and fruit P content. Leaf P content had a highly significant positive correlation with branch P content.

3.7. Correlation of C, N, P and Their Ratios in Different Organs of Male F. velutina in the Middle of the Growing Season

Unlike female plants, there were more significant correlations between the indices of elements and their ratios of different organs in male plants (Table 3). The leaf N content had a highly significant positive or negative correlation with other indices of C, N and P contents or their ratios (p < 0.01). Except for branch C, branch P and branch C/P, there was a highly significant correlation between leaf P content and other indices (p < 0.01). There were also highly significant correlations between branch C and branch P with many other indices (p < 0.01). There was a highly significant positive correlation between branch C content and leaf C content (p < 0.01), which was also different from that of female plants.

4. Discussion

Woody plants store nutrition in roots and in the bark of shoots and trunks [21]. During leaf unfolding in spring, inorganic N stored in the buds is allocated to new leaves, and as such, in the early growing season, the leaves of most autumn-deciduous tree species have relatively high N concentrations [22]. The seasonal stoichiometric dynamics of Larix principis-rupprechtii Mayr. showed that the leaf P concentrations were greatest in the early growing season [23]. Another study on seasonal variation in leaf nitrogen of Quercus serrata found that leaf N concentration peaked after bud burst, declined for two weeks shortly thereafter, and then remained constant for the remainder of the growing season [24]. Similar to the above-mentioned studies, the leaf C, N and P contents of the female and male plants of F. velutina all had the highest value in the early growing season.
In deciduous trees, leaves accumulate nutrition during the growing season, which is then continuously mobilized into woody tissues and fruits before leaf fall [25,26]. The branch N content of F. velutina in the early season was also lower than that in the late season. In contrast to the trend in leaf C, N and P, the fruit C, N and P of F. velutina all showed a gradually increasing trend in the growing season. The fruit C, N and P contents of F. velutina in the late growing season, especially from September to November, were all higher than in leaf and branch, due to the slowdown or cessation of leaf growth and the nutrient resorption at that time [27]. The contents of some mineral elements in deciduous trees markedly decrease in autumn because they are resorbed by the tree before leaf abscission [28]. In November, at the end of the growing season, the leaf N and P contents of the female and male plants of F. velutina were significantly lower than those in previous months.
The geometric mean of the leaf N/P ratio for 753 species in China was 14.4 [29], and the mean leaf N/P ratio of 154 deciduous woody plant species from the North-South Transect of East China was 12.76 [30]. The average leaf N/P ratio of 102 dominant species in the forest ecosystem of East China was 11.50 [31]. The leaf N/P of F. velutina in this study ranged from 6.60–11.62 during the growing season, which was lower than the mean value of other local species in China. The leaf N/P ratios higher than 16 indicated P limitation, lower than 14 indicated N limitation, and in between (14 < N/P < 16) indicated N and P co-limitation [32]. Therefore, the F. velutina stand in our study showed N limitation. The leaf N/P ratio increases with mean temperature and closeness to the equator because P is a major limiting nutrient in older tropical soils, and N is the major limiting nutrient in younger temperate and high-latitude soils [33]; the result from this study site (temperate zone) also supported this trend.
Female plants allocate more resources to reproduction, resulting in slower radial growth after reaching sexual maturity [34,35]. The dioecious plants usually have sex-specific resource requirements for reproduction (i.e., high carbon requirements for ovules and high nitrogen demands for pollen) [36]. Gender-specific differences in nutrient concentrations were found within dioecious species. The leaf N content of Rubus chamaemorus L. was found to be higher in males, particularly within 2–3 weeks after flowering [37]. Lower N concentration was also demonstrated in the females of Populus cathayana Rehd. and Acer negundo L. [38,39]. During the fruiting period of Pistacia lentiscus L., the production of current-year vegetative biomass and mineral mass (N, P, K) was higher in male than in female branches [40]. Generally, females need more P to support and maintain higher P utilization efficiency for fast growth to match their higher reproductive costs [41]. Similar to the above-mentioned results, the leaf N content of the female plants of F. velutina was lower than that of male plants in most months. However, the leaf C and P contents of female F. velutina were higher than those of male plants during most months. This result was consistent with the above hypothesis of the sex-specific nutrients requirements of dioecious plants [36].
Similar to the leaf N content, the branch N content of male plants of F. velutina was higher than that of female plants in most months. Contrary to the gender specificity of P content in leaves, the branch P content of female plants was slightly lower than that of male plants in most months. Female plants of F. velutina distributed more P resources to leaves and fruits in the growing season, which may result in lower P content in branches. Similar results were obtained for Pistacia lentiscus; the production of current-year vegetative biomass and P contents were higher in male than in female branches during the fruiting period of P. lentiscus [40]. Due to the small variation of C contents in leaf and branch at different growth stages, the sexual differences of the C/N and C/P of F. velutina leaf and branch were opposite to those of N and P in the growing season. Compared with females, the variation in the leaf N/P of male plants was smaller at different growth stages, which indicated that the reproductive growth of females affected the stability of leaf nutrient ratios.
Unlike female plants, the leaf C content of male plants had a highly significant positive correlation with branch C content. Compared with the female plants, male plants have less resources allocated to reproduction, and the leaves transport more resources directly to the branches; this may be the reason for the higher correlation between leaf C content and branch C content. The highly significant negative relationship between the leaf N content and fruit N content of female F. velutina plants exhibited a source-sink relationship between the leaf and fruit [42]. In the middle of the growing season, the leaf N was continuously transported to fruits and other organs, so the leaf N content gradually decreased, while the fruit N content gradually increased. The C/N and C/P ratios of the leaf, branch and fruit of female or male plants of F. velutina had a highly significant negative correlation with N or P content in the same organ, which showed that the variation of the C/N and C/P of leaf, branch and fruit was mainly determined by their N or P contents. This conclusion was similar to that reached by Reich and Oleksyn [33].
Compared to female plants of F. velutina, there were more significant correlations between the indices of N contents, P contents, the C/N/P ratios of leaves and the same indices of branches in male plants. For example, the leaf N content of male plants had a highly significant positive or negative correlation with other indices (p < 0.01). The leaf P content, branch N and branch P of males also had more significant correlations with other indices. In the middle growing season, the male plants were not involved in nutritional allocation for fruits; therefore, there were more significant correlations between the elements and ratios of branches and leaves.

5. Conclusions

This study analyzed the difference of stoichiometric characteristics between female and male F. velutina plants in urban forests of saline land. The main findings of this study include: (i) The leaf C, N and P contents of the female and male plants of F. velutina showed a similar seasonal trend. The leaf C, N and P contents of female and male plants were highest at the beginning of the growing season, and in November at the end of the growing season, the leaf N and P contents were significantly lower than before due to the nutrient resorption. The leaf C and P contents of females were slightly higher than those of males in most months; in contrast, the leaf N content was lower than that of male plants in most months. The above result was consistent with the hypothesis of sex-specific nutrients requirements of dioecious plants. (ii) The fruit C, N and P contents all gradually increased throughout the growing season. The fruit C, N and P contents in the late growing season were all higher than those in leaf and branch, due to the slowdown or cessation of leaf growth and the nutrient resorption at that time. In each month of the growing season, the N/P ratios of the fruit and branch of female plants were all relatively similar. (iii) Compared to the female plants of F. velutina, there were more significant correlations between the indices of the N and P contents and the C, N and P ratios of leaves and branches in males. (iv) The leaf N/P of F. velutina in this study ranged from 6.60 to 11.62 in the growing season; a value below14 indicated N limitation.

Author Contributions

A.S. and L.D. designed the study and collected the data. L.D., A.S. and N.C. were the major contributors in writing the manuscript. J.Z., L.P. and B.C. made substantial contributions to the data statistics and manuscript revision. All authors have read and agreed to the published version of the manuscript.

Funding

This research was financially supported by the Natural Science Foundation of Shandong Province (No. ZR2020MD007), the Major Scientific and Technological Innovation Projects of Shandong Province (No. 2017CXGC0316), and the Key Research and Development Program of Shandong Province (No. 2017GSF17113).

Data Availability Statement

Not applicable.

Acknowledgments

The staff of Shandong Key Laboratory of Eco-Environmental Science for Yellow River Delta of Binzhou University are thanked for technical support with the samples analysis.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Sterner, R.W.; Elser, J.J. Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere; Princeton University Press: Princeton, NJ, USA, 2002. [Google Scholar]
  2. Niklas, K.J.; Cobb, E.D. N, P, and C stoichiometry of Eranthis hyemalis (Ranunculaceae) and the allometry of plant growth. Am. J. Bot. 2005, 92, 1256–1263. [Google Scholar] [CrossRef] [PubMed]
  3. Wright, I.J.; Westoby, M. Nutrient concentration, resorption and lifespan: Leaf traits of Australian sclerophyll species. Funct. Ecol. 2003, 17, 10–19. [Google Scholar] [CrossRef] [Green Version]
  4. Akram, M.A.; Wang, X.T.; Hu, W.G.; Xiong, J.L.; Zhang, Y.H.; Deng, Y.; Ran, J.Z.; Deng, J.M. Convergent variations in the leaf traits of desert plants. Plants 2020, 9, 990. [Google Scholar] [CrossRef] [PubMed]
  5. Akram, M.A.; Zhang, Y.H.; Wang, X.T.; Shrestha, N.; Malik, K.; Khan, I.; Ma, W.J.; Sun, Y.; Li, F.; Ran, J.Z.; et al. Phylogenetic independence in the variations in leaf functional traits among different plant life forms in an arid environment. J. Plant Physiol. 2022, 272, 153671. [Google Scholar] [CrossRef]
  6. Rocheleau, A.F.; Houle, G. Different cost of reproduction for the males and females of the rare dioecious shrub Corema conradii (Empetraceae). Am. J. Bot. 2001, 88, 659–666. [Google Scholar] [CrossRef]
  7. Li, J.Y.; Dong, T.F.; Guo, Q.X.; Zhao, H.X. Populus deltoides females are more selective in nitrogen assimilation than males under different nitrogen forms supply. Trees-Struct. Funct. 2015, 29, 143–159. [Google Scholar] [CrossRef]
  8. Obeso, J.R. The costs of reproduction in plants. New Phytol. 2002, 155, 321–348. [Google Scholar] [CrossRef]
  9. Zeng, D.H.; Chen, G.S. Ecological stoichiometry: A science to explore the complexity of living systems. Chin. J. Ecol. 2005, 29, 1007–1019. [Google Scholar]
  10. Elser, J.J.; Fagan, W.F.; Kerkhoff, A.J.; Swenson, N.G.; Enquist, B.J. Biological stoichiometry of plant production: Metabolism, scaling and ecological response to global change. New Phytol. 2010, 186, 593–608. [Google Scholar] [CrossRef] [Green Version]
  11. Xia, C.X.; Yu, D.; Wang, Z.; Xie, D. Stoichiometry patterns of leaf carbon, nitrogen and phosphorous in aquatic macrophytes in eastern China. Ecol. Eng. 2014, 70, 406–413. [Google Scholar] [CrossRef]
  12. Huang, X.M.; Ma, Y.H.; Dong, T.F. Stoichiometric characteristics of C, N and P in the leaf of dioecious plant Cercidiphyllum japonicum. J. China West. Norm. Univ. (Nat. Sci.) 2019, 40, 332–338. [Google Scholar]
  13. Kinga, N.D.; Giertych, M.J.; Thomas, P.; Iszkulo, G. Males and females of Juniperus communis L. And Taxus baccata L. show different seasonal patterns of nitrogen and carbon content in needles. Acta Physiol. Plant 2017, 39, 191. [Google Scholar]
  14. Blake-Mahmud, J.; Struwe, L. Death, sex, and sugars: Variations in nonstructural carbohydrate concentrations in a sexually plastic tree. Am. J. Bot. 2020, 107, 375–382. [Google Scholar] [CrossRef] [PubMed]
  15. Du, Z.Y.; Wang, Q.H.; Xing, S.J.; Liu, F.C.; Ma, B.Y.; Ma, H.L.; Liu, D.X. Fine root distribution, characteristics and rhizosphere soil properties in a mixed stand of Robinia pseudoacacia and Fraxinus velutina in a saline soil. Silva Fenn. 2013, 47, 970. [Google Scholar] [CrossRef]
  16. Li, T.; Sun, J.K.; Li, C.R.; Lu, J.H.; Xia, J.B. Cloning and expression analysis of the FvNCED3 gene and its promoter from ash (Fraxinus velutina). J. For. Res. 2019, 30, 471–482. [Google Scholar] [CrossRef]
  17. Song, A.Y.; Dong, L.S.; Chen, J.X.; Peng, L.; Liu, J.T.; Xia, J.B.; Chen, Y.P. Comparation of seasonal dynamics of mineral elements contents indifferent organs of male and female plants of Fraxinus velutina. Sci. Silva. Sin. 2019, 10, 162–170. [Google Scholar]
  18. John, M. Colorimetric determination of phosphorus in soil and plant materials with ascorbic acid. Soil. Sci. 1970, 109, 214–220. [Google Scholar] [CrossRef]
  19. Scott, E.; Prater, C.; Norman, E.; Baker, B.; Evans-White, M.; Scott, J. Leaf-litter stoichiometry is affected by streamwater phosphorus concentrations and litter type. Freshw. Sci. 2013, 32, 753–761. [Google Scholar] [CrossRef] [Green Version]
  20. Kosovka, O.D.; Vesna, M.; Marina, R.; Mila, L. Correlation between the degree of conversion and the elution of leachable components from dental resin-based cements. J. Serb. Chem. Soc. 2011, 76, 1307–1323. [Google Scholar]
  21. Titus, S.J.; Kang, S.M. Nitrogen metabolism, translocation, and recycling in apple trees. Hortic. Rev. 1982, 4, 204–206. [Google Scholar]
  22. Dawson, J.O.; Funk, D.T. Seasonal change in foliar nitrogen concentration of Alnus glutinosa. For. Sci. 1981, 27, 239–243. [Google Scholar]
  23. Li, H.L.; Crabbe, M.; Xu, F.L.; Wang, W.L.; Ma, L.H.; Niu, R.L.; Gao, X.; Li, X.X.; Zhang, P.; Ma, X.; et al. Seasonal variations in carbon, nitrogen and phosphorus concentrations and C:N:P stoichiometry in different organs of a Larix principis-rupprechtii Mayr. plantation in the Qinling Mountains, China. PLoS ONE 2017, 12, e0185163. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  24. Migita, C.; Chiba, Y.; Tange, T. Seasonal and spatial variations in leaf nitrogen content and resorption in a Quercus serrata canopy. Tree Physiol. 2007, 27, 63–70. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  25. Inagaki, M.; Kamo, K.; Miyamoto, K.; Titin, J.; Jamalung, L.; Lapongan, J.; Miura, S. Nitrogen and phosphorus retranslocation and N:P ratios of litterfall in three tropical plantations: Luxurious N and efficient P use by Acacia mangium. Plant Soil. 2011, 41, 295–307. [Google Scholar] [CrossRef]
  26. Weinbaum, S.A.; Klein, I.; Broadbent, F.E.; Micke, W.C. Effects of time of nitrogen application and soil texture on the availability of isotopically labeled fertilizer nitrogen to reproductive and vegetative tissue of mature almond trees. J. Am. Soc. Hortic. Sci. 1984, 109, 339–343. [Google Scholar] [CrossRef]
  27. Han, Q.M.; Kabeya, D.; Inagaki, Y. Influence of reproduction on nitrogen uptake and allocation to new organs in Fagus crenata. Tree Physiol. 2017, 37, 1436–1443. [Google Scholar] [CrossRef] [Green Version]
  28. Grassi, G.; Vicinelli, E.; Ponti, F.; Cantoni, L.; Magnani, F. Seasonal and interannual variability of photosynthetic capacity in relation to leaf nitrogen in a deciduous forest plantation in northern Italy. Tree Physiol. 2005, 25, 349–360. [Google Scholar] [CrossRef]
  29. Han, W.X.; Fang, J.Y.; Guo, D.L.; Zhang, Y. Leaf nitrogen and phosphorus stoichiometry across 753 terrestrial plant species in China. New Phytol. 2005, 168, 377–385. [Google Scholar] [CrossRef]
  30. Ren, S.J.; Yu, G.R.; Tao, B.; Wang, S.Q. Leaf nitrogen and phosphorus stoichiometry across 654 terrestrial plant species in NSTEC. Environ. Sci. 2007, 28, 2665–2673. [Google Scholar]
  31. Ren, S.J.; Yu, G.R.; Jiang, C.M.; Fang, H.J.; Sun, X.M. Stoichiometric characteristics of leaf carbon, nitrogen, and phosphorus of 102 dominant species in forest ecosystems along the North-South Transect of East China. Chin. J. Appl. Ecol. 2012, 23, 581–586. [Google Scholar]
  32. Koerselman, W.; Meuleman, A. The vegetation N:P ratio: A new tool to detect the nature of nutrient limitation. J. Appl. Ecol. 1996, 33, 1441–1450. [Google Scholar] [CrossRef]
  33. Reich, P.B.; Oleksyn, J. Global patterns of plant leaf N and P in relation to temperature and latitude. Proc. Natl. Acad. Sci. USA 2004, 101, 11001–11006. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  34. Banuelos, M.J.; Obeso, J.R. Resource allocation in the dioecious shrub Rhamnus alpinus: The hidden costs of reproduction. Evol. Ecol. Res. 2004, 6, 397–413. [Google Scholar]
  35. Montesinos, D.; Luis, M.D.; Verdu, M.; Ravento, J.; Garcia-fayos, P. When, how and how much: Gender-specific resource-use strategies in the dioecious tree Juniperus thurifera. Ann. Bot. 2006, 98, 885–889. [Google Scholar] [CrossRef] [PubMed]
  36. Tonnabel, J.; David, P.; Pannell, J.R. Sex-specific strategies of resource allocation in response to competition for light in a dioecious plant. Oecologia 2017, 185, 675–686. [Google Scholar] [CrossRef] [Green Version]
  37. Agren, J. Sexual differences in biomass and nutrient allocation in the dioecious Rubus chamaemorus. Ecology 1988, 69, 962–973. [Google Scholar] [CrossRef]
  38. Chen, L.H.; Dong, T.F.; Duan, B.L. Sex-specific carbon and nitrogen partitioning under N deposition in Populus cathayana. Trees 2014, 28, 793–806. [Google Scholar] [CrossRef]
  39. Dawson, T.; Ehleringer, J. Gender-specific physiology, carbon isotope discrimination, and habitat distribution in boxelder, Acer negundo. Ecology 1993, 74, 798–815. [Google Scholar] [CrossRef]
  40. Milla, R.; Castro-Díez, P.; Maestro-Martínez, M.; Montserrat-Martí, G. Costs of reproduction as related to the timing of phenological phases in the dioecious shrub Pistacia lentiscus L. Plant Biol. 2006, 8, 103–111. [Google Scholar] [CrossRef] [Green Version]
  41. Xia, Z.C.; He, Y.; Zhou, B.; Korpelainen, H.; Li, C.Y. Sex-related responses in rhizosphere processes of dioecious Populus cathayana exposed to drought and low phosphorus stress. Environ. Exp. Bot. 2020, 175, 104049. [Google Scholar] [CrossRef]
  42. Proietti, P. Effect of fruiting on leaf gas exchange in olive (Olea europaea L). Photosynthetica 2000, 8, 397–402. [Google Scholar] [CrossRef]
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Figure 1. Monthly dynamic of C (a), N (b), P (c) contents in different organs of female plants of F. velutina. Note: Means of different months not sharing the same letter indicated significant differences at an alpha level of 0.05, according to an LSD test.
Figure 1. Monthly dynamic of C (a), N (b), P (c) contents in different organs of female plants of F. velutina. Note: Means of different months not sharing the same letter indicated significant differences at an alpha level of 0.05, according to an LSD test.
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Forests 14 00064 g002 550
Figure 2. Monthly dynamic of C (a), N (b), P (c) contents in different organs of male plants of F. velutina. Note: Means of different months not sharing the same letter indicated significant differences at an alpha level of 0.05, according to an LSD test.
Figure 2. Monthly dynamic of C (a), N (b), P (c) contents in different organs of male plants of F. velutina. Note: Means of different months not sharing the same letter indicated significant differences at an alpha level of 0.05, according to an LSD test.
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Forests 14 00064 g003a 550Forests 14 00064 g003b 550
Figure 3. Monthly dynamic of C/N (a), C/P (b), N/P (c) ratios in different organs of female plants of F. velutina. Note: Means of different months not sharing the same letter indicated significant differences at an alpha level of 0.05, according to an LSD test.
Figure 3. Monthly dynamic of C/N (a), C/P (b), N/P (c) ratios in different organs of female plants of F. velutina. Note: Means of different months not sharing the same letter indicated significant differences at an alpha level of 0.05, according to an LSD test.
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Forests 14 00064 g004a 550Forests 14 00064 g004b 550
Figure 4. Monthly dynamic of C/N (a), C/P (b), N/P (c) ratios in different organs of male plants of F. velutina. Note: Means of different months not sharing the same letter indicated significant differences at an alpha level of 0.05, according to an LSD test.
Figure 4. Monthly dynamic of C/N (a), C/P (b), N/P (c) ratios in different organs of male plants of F. velutina. Note: Means of different months not sharing the same letter indicated significant differences at an alpha level of 0.05, according to an LSD test.
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Forests 14 00064 g005a 550Forests 14 00064 g005b 550
Figure 5. Comparation of C (a), N (b), P (c) contents in leaf of female and male plants of F. velutina during the growing season. Note: Means not sharing the same letter of female and male plants in the same month indicated significant differences between males and females at an alpha level of 0.05, according to one-way ANOVA.
Figure 5. Comparation of C (a), N (b), P (c) contents in leaf of female and male plants of F. velutina during the growing season. Note: Means not sharing the same letter of female and male plants in the same month indicated significant differences between males and females at an alpha level of 0.05, according to one-way ANOVA.
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Figure 6. Comparation of C (a), N (b), P (c) content in branch of female and male plants of F. velutina during the growing season. Note: Means not sharing the same letter of female and male plants in the same month indicated significant differences between males and females at an alpha level of 0.05, according to one-way ANOVA.
Figure 6. Comparation of C (a), N (b), P (c) content in branch of female and male plants of F. velutina during the growing season. Note: Means not sharing the same letter of female and male plants in the same month indicated significant differences between males and females at an alpha level of 0.05, according to one-way ANOVA.
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Forests 14 00064 g007 550
Figure 7. Comparation of C/N (a), C/P (b), N/P (c) ratios in leaf of female and male plants of F. velutina during the growing season. Note: Means not sharing the same letter of female and male plants in the same month indicated significant differences between males and females at an alpha level of 0.05, according to one-way ANOVA.
Figure 7. Comparation of C/N (a), C/P (b), N/P (c) ratios in leaf of female and male plants of F. velutina during the growing season. Note: Means not sharing the same letter of female and male plants in the same month indicated significant differences between males and females at an alpha level of 0.05, according to one-way ANOVA.
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Figure 8. Comparation of C/N (a), C/P (b), N/P (c) ratios in branch of female and male plants of F. velutina during the growing season. Note: Means not sharing the same letter of female and male plants in the same month indicated significant differences between males and females at an alpha level of 0.05, according to one-way ANOVA.
Figure 8. Comparation of C/N (a), C/P (b), N/P (c) ratios in branch of female and male plants of F. velutina during the growing season. Note: Means not sharing the same letter of female and male plants in the same month indicated significant differences between males and females at an alpha level of 0.05, according to one-way ANOVA.
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Table
Table 1. Average value of soil property indices of six random soil samples in the plantation of F. velutina.
Table 1. Average value of soil property indices of six random soil samples in the plantation of F. velutina.
Bulk Density (g cm−3)pHSoil Organic Matter (g kg−1)Alkali-Hydrolyzed Nitrogen (mg kg −1)Available Phosphorus (mg kg−1)Available Potassium (mg kg−1)Salt Content (g kg−1)
1.387.9013.3619.7535.2696.522.51
Table
Table 2. The correlation of C, N and P contents and their ratios of different organs of female plants of F. velutina.
Table 2. The correlation of C, N and P contents and their ratios of different organs of female plants of F. velutina.
IndicesLeaf CLeaf NLeaf PBranch CBranch NBranch PFruit CFruit NFruit P
Leaf N0.334 *
Leaf P0.220−0.006
Branch C0.1800.399 *−0.055
Branch N0.1970.2780.1950.034
Branch P0.243−0.1540.448 **−0.0130.303
Fruit C0.014−0.3220.022−0.0400.2030.320
Fruit N−0.197−0.446 **−0.071−0.395 *0.167−0.1550.304
Fruit P−0.177−0.520 **0.167−0.385 *0.0220.1110.1590.616 **
Leaf C/N−0.307−0.953 **−0.046−0.283−0.334 *0.0970.3130.339 *0.520 **
Leaf C/P−0.045−0.008−0.862 **0.082−0.123−0.383 *0.0760.164−0.175
Leaf N/P0.0880.653 **−0.660 **0.2770.116−0.408 *−0.156−0.156−0.482 **
Branch C/N−0.271−0.222−0.2530.035−0.954 **−0.293−0.177−0.174−0.059
Branch C/P−0.1410.343 *−0.3150.110−0.218−0.912 **−0.362 *0.046−0.098
Branch N/P−0.0510.453 **−0.2170.1070.284−0.723 **−0.2420.092−0.007
Fruit C/N0.1940.407 *0.0330.388 *−0.1440.249−0.043−0.936 **−0.605 **
Fruit C/P0.1830.432 **−0.1760.3100.013−0.0170.110−0.554 **−0.942 **
Fruit N/P−0.108−0.065−0.266−0.1870.152−0.342 *0.2180.699 **−0.115
Note: *, ** denote significance at the 0.05, 0.01 test level, respectively. In this text, the “significant” and “highly significant” correlations refer to significance at the 0.05 and 0.01 test levels, respectively. The correlation coefficients between the ratios of elements in different organs are not listed in the table.
Table
Table 3. The correlation of C, N and P contents and their ratios of different organs of male plants of F. velutina.
Table 3. The correlation of C, N and P contents and their ratios of different organs of male plants of F. velutina.
IndicesLeaf CLeaf NLeaf PBranch CBranch NBranch P
Leaf N0.329 *
Leaf P−0.256−0.591 **
Branch C0.664 **0.551 **−0.132
Branch N−0.0490.632 **−0.487 **0.1
Branch P0.067−0.495 **0.304−0.005−0.226
Leaf C/N−0.281−0.973 **0.650 **−0.475 **−0.653 **0.475 **
Leaf C/P0.2310.596 **−0.944 **0.1520.577 **−0.342 *
Leaf N/P0.2010.885 **−0.817 **0.348 *0.717 **−0.500 **
Branch C/N0.144−0.571 **0.458 **0.014−0.960 **0.189
Branch C/P0.00040.594 **−0.2960.1510.272−0.942 **
Branch N/P−0.0810.707 **−0.437 **0.0930.676 **−0.822 **
Note: *, ** denote significance at the 0.05, 0.01 test level, respectively. In this text, the “significant” and “highly significant” correlations refer to significance at the 0.05 and 0.01 test level, respectively. The correlation coefficients between the ratios of elements in different organs are not listed in the table.
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Dong, L.; Song, A.; Zhang, J.; Peng, L.; Cheng, N.; Cao, B. Comparison of C, N and P Stoichiometry in Different Organs of Fraxinus velutina. Forests 2023, 14, 64. https://doi.org/10.3390/f14010064

AMA Style

Dong L, Song A, Zhang J, Peng L, Cheng N, Cao B. Comparison of C, N and P Stoichiometry in Different Organs of Fraxinus velutina. Forests. 2023; 14(1):64. https://doi.org/10.3390/f14010064

Chicago/Turabian Style

Dong, Linshui, Aiyun Song, Jianfeng Zhang, Ling Peng, Nannan Cheng, and Banghua Cao. 2023. "Comparison of C, N and P Stoichiometry in Different Organs of Fraxinus velutina" Forests 14, no. 1: 64. https://doi.org/10.3390/f14010064

APA Style

Dong, L., Song, A., Zhang, J., Peng, L., Cheng, N., & Cao, B. (2023). Comparison of C, N and P Stoichiometry in Different Organs of Fraxinus velutina. Forests, 14(1), 64. https://doi.org/10.3390/f14010064

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