Typical garden tree species are very representative in studying material cycle of urban ecosystem. To study the response of nutrient storage and resorption strategies of different life-form garden tree species to soil nutrients is the key to the sustainability of the urban garden ecosystem. In this research, 9 sample trees out of every 40 garden tree species, which were classified into 2 life forms, were selected for repeated sampling. Nitrogen (N) and phosphorus (P) concentrations in green and senesced leaves and soil nutrient concentrations were investigated, respectively. By comparing nutrient concentrations and resorption of different life-form tree species, the utilization strategies of soil nutrients by different life-form tree species were further analysed. N concentration was substantially higher in deciduous plants with green and senesced leaves than in evergreen ones. Green leaves of deciduous plants had much greater P concentrations than those of evergreen plants, although the difference between the two was not statistically significant. Leaf N:P between different life forms was less than 14, showing a tendency to N limitation. Nitrogen resorption efficiency (NRE) and phosphorous resorption efficiency (PRE) in deciduous plants were significantly higher than in evergreen plants. NRE in deciduous plants was significantly positively correlated with PRE, but not significant in evergreen plants. NuRE of evergreen plants increased as soil N and P concentrations increased, but NuRE of deciduous plants dropped as soil N and P concentrations increased. Compared with deciduous plants, evergreen plants were more sensitive to soil N and P concentrations. These findings have important implications for urban garden trees management practices in this region.
Article
Leaf nutrient resorption and response to soil nutrient availability of different life-form urban garden trees
https://doi.org/10.21203/rs.3.rs-2206591/v1
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Garden tree species
green and senesced leaves
life form
soil nutrient
nutrient resorption
nutrient limitation
Before shedding leaves, a plant tissue or organ transfers part of its nutrients (mostly nitrogen and phosphorus) to other living tissues or organs. This process is known as nutrient resorption [1]. This technique, which is regarded as a crucial nutrient conservation mechanism, can increase the efficiency of nutrient usage, increase the retention period of nutrients in plants and lessen their reliance on soil nutrients [2]. Through senesced leaves, leaf nutrient resorption efficiency offers feedback on nutrient cycle and plant output, reflecting how individual plants respond to nutrient constraint [3].
The reasons for the changes in leaf nutrient resorption between species with various life forms are yet unknown [4]. At the global scale, nitrogen resorption efficiency (NRE) and phosphorous resorption efficiency (PRE) are lower in evergreen plants than in deciduous plants [5]. NRE and PRE were shown to be higher in conifers than in broadleaved trees in a study of 137 woody species in six different forest types in northern China [6]. But some scholars also believed that there were no differences in nutrient resorption between deciduous and evergreen plants [7].
It is believed that nutrient resorption is closely related to soil nutrient availability [8] and stoichiometry in the environment [9]. Studies have showed that nutrient resorption efficiency (NuRE) decreased with the increase of available soil nutrients [10]. Nutrient transport between soil and plants heavily depended on the decomposition of leave litter and the supply of soil nutrients [11]. In addition, the rate of nutrient loss in senesced leaves is thought to be a feedback of the dynamics of soil nutrition. While nutrient concentrations remained in senesced leaves in turn affect their decomposition rates and soil nutrient availability [9]. However, there were differences in soil nutrient absorption by leaf nutrient resorption in different life forms. NRE and PRE in evergreen plants, which were usually dominated by barren environments [12], are similar to or even lower than deciduous plants on nutrient-rich soils (1996, Aerts). Someone believed that plant functional types contributed more to the change of NRE, while climate and soil had a greater impact on the change of PRE [6]. But the difference needs to be further clarified.
Urban Garden Trees (UGT) is an important part of urban green space (UGS) [13]. The reasonable choice and use of garden trees are the key to designing the precise cultivation and opration measures, building a conservation-minded landscape and “ecological garden city”, improving the urban environment and ecosystem stability [14]. It is also the basis of the urban area to achieve "carbon emission peak and carbon neutrality" [15] and the only way to promote sustainable urban development [16] [17]. However, due to the increasing human disturbance, the soil nutrient dynamic balance of urban ecosystem has been greatly changed or even destroyed in recent years [18] and the ecological strategies of plants, especially the nutrient strategie, changed correspondingly. However, the strategies of different tree species have not been thoroughly studied [4].
Studying the nutrient utilization strategies between different life forms can contribute to the understandings of the relationship between nutrient use policies among different tree types and soil, and exploring the adaptability of different plant types and the nutrient cycle in urban ecosystems. By investigating the leaves and soil of 40 typically selected garden tree species in Taiyuan city, and studying the relationship between green leaves, senesced leaves and soil nutrient concentrations and N:P, we aim to propose a nutrient cycling mechanism from stoichiometric perspective.
We hypothesized that:
1. Different life forms plants had different N and P absorption strategies and the NuRE of evergreen plants was lower than deciduous plants.
2. There exsisted different nutrient limitation between evergreen and deciduous plants.
3. Evergreens plants were more sensitive to soil nutrients than deciduous plants.
2.1. N, P concentrations and N:P in green and senesced leaves between two life forms
N, P concentrations and N:P in green leaves were significantly higher in 40 typical garden tree species than those in senesced leaves, respectively. There were substantial differences between N, P concentrations and N:P in green leaves between different life forms. And senesced leaves between different life forms exsited significant differences in N concentration and N:P, and insignificant difference in P concentration. Additionally, except for P concentration in senesced leaves, N, P concentrations and N:P in evergreen plants were significantly lower than in deciduous plants (Table 1).
|
Leaves |
Life form |
n |
N (g·kg− 1) |
P (g·kg− 1) |
N:P |
|---|---|---|---|---|---|
|
Green leaves |
Evergreen |
18 |
6.38 ± 1.60a |
2.65 ± 0.43a |
2.45 ± 0.69a |
|
Deciduous |
102 |
14.61 ± 6.52b |
2.94 ± 0.70b |
5.04 ± 1.99b |
|
|
All |
120 |
13.38 ± 6.72A |
2.90 ± 0.68A |
4.65 ± 2.07A |
|
|
Senesced leaves |
Evergreen |
18 |
3.18 ± 0.44a |
1.75 ± 0.36a |
1.88 ± 0.47a |
|
Deciduous |
102 |
5.93 ± 2.65b |
1.61 ± 0.36a |
3.78 ± 1.70b |
|
|
All |
120 |
5.51 ± 2.64B |
1.63 ± 0.37B |
3.50 ± 1.72B |
2.2. NRE, PRE and their correlated relationship between different life forms
NRE and PRE of evergreen and deciduous plants were (56.13 ± 13.07)% and (41.14 ± 16.98)%, respectively. PRE was significantly lower than NRE. NRE and PRE were significantly different between evergreen and deciduous plants, and those of evergreen plants were significantly lower than deciduous plants (Fig. 1). NRE was significantly positively correlated with PRE among deciduous plants (P < 0.01) (Fig. 2). However, NRE had no obvious relationship with PRE among evergreen plants.
2.3. Soil nutrition concentrations
There were significant differences in nutrient concentrations among different trees (Appendix Table S1). The soil pH and N:P of evergreen plants were lower than those of deciduous plants. And soil TN, TP, NH4+-N, NO3−-N, NO2−-N and AP concentrations of evergreen plants were higher than those of deciduous plants, but there were no significant differences (Table 2).
|
Life form |
n |
pH |
TN (g·kg− 1) |
TP (g·kg− 1) |
TN:TP |
NH4+-N (mg·kg− 1) |
NO3−-N (mg·kg− 1) |
NO2−-N (mg·kg− 1) |
AP (mg·kg− 1) |
|---|---|---|---|---|---|---|---|---|---|
|
Evergreen |
18 |
8.45 ± 0.12 |
0.63 ± 0.20 |
0.60 ± 0.15 |
1.11 ± 0.40 |
12.45 ± 2.15 |
14.84 ± 8.25 |
0.15 ± 0.06 |
7.39 ± 1.74 |
|
Deciduous |
102 |
8.48 ± 0.17 |
0.59 ± 0.27 |
0.53 ± 0.16 |
1.26 ± 0.96 |
11.50 ± 2.26 |
13.93 ± 7.80 |
0.14 ± 0.05 |
7.19 ± 1.81 |
2.4. Relationship between leaves indexes and soil nutrients in different life forms
NRE and PRE in different life forms were distinctly correlated with soil nutrient concentrations and N:P. For evergreen plants, NRE and Ngr had a obviously positive relationship with soil N (Fig. 3a-b). NRE, Ngr, Pgr and Psen had a significantly positive relationship with soil N:P (Fig. 3j-l, n). For deciduous plants, NRE had a greatly negative relationship with soil N (Fig. 3a) and PRE had a similar relationship with soil P (Fig. 3d). Nsen had a obviously positive relationship with soil N, NH4+-N, NO3−-N, NO2−-N and N:P (Fig. 3c, f, h, i, m), respectively. Ngr had a distinctly positive relationship with soil NO3−-N (Fig. 3g). Psen had a significantly positive relationship with soil P (Fig. 3e).
For evergreen plants, the explanations of Ngr, Pgr, Nsen and Psen in the first and second axes of RDA were 39.36% and 7.634%, respectively. The cumulative amount of explanation was 46.994% (Fig. 4a). Ngr, Pgr, Nsen and Psen were significantly correlated with soil TN, and its explanation was 21.4% (Fig. 4a). The explanations of NRE and PRE in the first and second axes of RDA were 32.89% and 8.814%, respectively. The cumulative amount of explanation was 41.704% (Fig. 4b).
For deciduous plants, the explanations of Ngr, Pgr, Nsen and Psen in the first and second axes of RDA were 22.76% and 1.058%, respectively. The cumulative amount of explanation was 23.818% (Fig. 4c). Ngr, Pgr, Nsen and Psen were substantially associated with soil TN and NO3−-N, and their explanations were 1.3% and 20.6%, respectively (Fig. 4c). The explanations of NRE and PRE in the first and second axes of RDA were 8.423% and 1.165%, respectively. The cumulative amount of explanation was 9.588% (Fig. 4d). PRE and NRE were distinctly related to the soil TP, and their explanation was 5.6% (Fig. 4d). All the data could accurately reflect the relationship between leaves’ Ngr, Pgr, Nsen, Psen, NuRE and soil nutrients.
3.1 N, P concentrations and N:P in leaves
Leaf nutrient concentration is a key indicator of plant nutritional status [19]. In our research, the green leaf N concentration (13.38 g·kg− 1) was lower than the average N concentration (17.57 g·kg− 1) of woody plants in NSTEC (North-South transect of eastern China) [20]. Plants mainly obtained P and N from the soil [21, 22]. Leaves in urban green space are removed regularly every year, resulting in serious soil N loss. Therefore, the soil N concentration in this area was low (TN = 0.61 g·kg− 1) and leaf N concentration was further reduced. Since plants in southern China were generally limited by P and the soil P concentration in northern China was relatively sufficient, leaf P concentration (2.90 g·kg− 1) in this area was relatively higher than that of woody plants (1.39 g·kg− 1) in NSTEC [20].
In this research, green leaf P and N concentrations in deciduous plants were significantly higher than in evergreen plants. This might be attributed to the fact that deciduous plants need to accumulate more N and P in a short time to complete growth activities. Due to the longer leaf life cycle of evergreen plants, they took much more time to conserve nutrients [23]. Compared with evergreen plants, deciduous plants had higher levels of litter decomposition and nutrient absorption [24]. Senesced leaf N concentration in evergreen plants was significantly lower than in deciduous plants, indicating that N utilization efficiency was higher than P utilization efficiency [6] in this area.
In most terrestrial ecosystems, the availability of N and P limited the growth of plants. The concentrations of N and P in green leaves and the N:P could be used as a standard of plant nutritional limitation [25]. Plants were limited by P when N:P > 16 and P concentration < 1.0 mg·g− 1 in green leaves. While plants were limited by N when N:P < 14 and N concentration < 20.0 mg·g− 1. The leaf N:P in two life forms was less than 14, and N concentration was less than 20.0 mg·g− 1 in most plants, indicating that the growth of garden trees in Taiyuan might be limited by N. In addition, N:P in deciduous plants was higher than in evergreen plants, showing that N limitation was different between evergreen and deciduous plants, which was consistent with hypothesis 2 put forward.
3.2 The differences of NRE and PRE in two life forms
Senesced leaves fall to the ground and gradually break down into inorganic nutrients due to physical and microbiological processes, and these re-mineralized nutrients will eventually be absorbed by plants (biogeochemical cycle) [26]. NRE (56.13%) was higher than PRE (41.14%), indicating plant absorption of N was higher than P. But they were lower than the NRE and PRE (62.1% and 64.9%) of global terrestrial forest ecosystems. It might be due to the differences in trees or habitats selected in the research. It could also be explained by the fact that when plants were restricted by N, they tended to accomplish total N absorption but inadequate P absorption [19].
Compared with evergreen plants, deciduous plants had much higher NRE and PRE indicating nutrient utilization in evergreen plants was lower than that in deciduous plants [27]. P resorption variation is more affected by climate and soils. While N resorption variance has more to do with plant functional type [6]. Evergreen plants, a type of highly specialized plants, have developed an adaptation technique to flourish in nutrient-poor soil [28]. In barren soil, extending evergreen plants’ leaves lifespans can enable the growth rate to its maximum [29], and the nutrient losses to its minimum during leaves senescencing and shedding [30]. During the growth season, deciduous plants produce more leaves, and they shed their leaves annually [31]. Thus, deciduous plants often invest more nutrients to support rapid growth during shorter growing seasons [32]. Deciduous plants had much higher NRE and PRE than evergreen plants. Additionally, the variation in decomposability-related characteristics of the litter (such as lignin: N and N:P) and the habitat climate (temperature/precipitation) may work in conjunction to affect the availability of soil nutrients and, consequently, the levels of NRE and PRE in evergreen and deciduous plants [33].
In addition, in deciduous plants, NRE was positively associated with PRE, indicating that N absorption rises concurrently with P absorption. This was a crucial premise for the stoichiometry control [19]. It further showed that deciduous plantes had a synergistic effect on N and P. A meta-analysis by Aerts [30] reported NRE and PRE also had a strong association with one another.
3.3 Relationship between leaf Ngr, Pgr, Nsen, Psen, NuRE and soil nutrients in two life forms
Soil nutrient availability and leaf nutrient status are considered to be the important control factors for nutrient absorption process[34, 35]. Our findings demonstrated that soil nutrients had a considerable impact on leaf N and P concentrations as well as NuRE in two life forms. The availability of N and P had a significant impact on how soil nutrients were utilized, which had an impact on NuRE [36].
For evergreen plants, NRE and Ngr were positively correlated with soil TN, indicating that evergreen plants would not reduce resorption level to adapt to the increase in soil N concentration. And the increase of NRE was mainly due to the decrease of Ngr. We predicted that evergreen plants tended to store a large amount of N in green leaves when soil N supply was sufficient or possibly N-limited, while N in senesced leaves was almost unaffected, thus improving NRE. The ratio of soil N:P can be used as a measure for N-saturation, showing the availability of nutrients for plant growth [37]. Pgr and Psen were positively related with soil N:P, indicating that evergreen plants adopted a nutrient utilization strategy with high concentration and high return to maintain normal physiological activities when soil P was relatively scarce compared with N. NRE and Ngr in evergreen plants were positively associated with soil N:P, and RDA (Fig. 4a) showed that soil TN had the highest explanation, which indicated that soil TN supply was the key factor for affecting N and P concentrations in leaves of evergreen plants.
For deciduous plants, NRE was negatively correlated with soil TN while PRE was negatively associated with soil TP, indicating that NRE and PRE decreased with the increase of soil TN and TP. We concluded that deciduous plants did not need higher resorption efficiency to maintain N and P concentrations when N and P supply in the soil was sufficient. The result is consistent with Kobe [38]. Nsen was positively associated with soil N in various forms and N:P, indicating that Nsen increased with the rise of soil N concentration and availability. Deciduous plants mainly affected Nsen through soil N concentration, which further affected NRE. The dominating soil factors for N and P concentrations in deciduous plants were soil TN and NO3−-N (Fig. 4c), and soil TP was the main soil factor for affecting NuRE (Fig. 4d), indicating the soil N mainly influenced leaf N, P concentrations while the soil P mainly affected leaf NuRE in deciduous plants. Evergreen plants explained more soil accumulation than deciduous plants, demonstrating that evergreen plants were more sensitive to soil N and P concentrations than deciduous plants.
This research presents an advanced understanding of N and P nutrient absorption strategies, and the soil nutrient response to garden tree species of different life forms in urban ecosystems. Compared with senesced leaves, N and P concentrations in green leaves were significantly higher. N concentration was much higher in deciduous plants with green and senesced leaves than it was in evergreen plants. Compared with evergreen plants, deciduous plants had much higher levels of P in their green leaves. While P concentration in senesced leaves of different life forms existed unsignificant difference. Two life forms showed a tendency to N limitation with different degrees. Compared with evergreen plants, deciduous plants had much higher NRE and PRE. NRE in deciduous plant was significantly positively correlated with PRE. The NuRE of evergreen plants grew whereas that of deciduous plants dropped when soil N and P concentrations rose. The main element influencing leaf N and P concentrations in evergreen plants was soil TN supply. Soil N mainly influenced leaf N and P concentrations while soil P mainly influenced NuRE in deciduous plants. Compared with deciduous plants, evergreen plants were more sensitive to soil N and P concentrations. Our findings can help explain how N and P absorption fluctuate and how UGT reacts to global change. Furthermore, the findings offer a theoretical foundation for the development of ecological garden cities and can be used to incorporate these nutrient absorption processes into upcoming biogeochemical models.
5.1. Study site
The research was done in Taiyuan City, Shanxi Province, China, between the latitudes of 37.27 °N and 38.25 °N. Taiyuan is located in the central Shanxi Province with its three sides (west, north and east) surrounded by the mountains and one side (south) facing Jinzhong Basin. The overall topography is high in the north and low in the south and the Fenhe River goes through the city. With an average annual temperature of 9.5 ℃ and 456 millimetres of precipitation, the city has a warm temperate continental monsoon climate. Zonal soil type is mainly brown soil. Site condition diversities in urban area are mainly reflected in the limited difference of groundwater level and soil characteristics caused by river distance.
5.2. Experimental design
Based on the number and frequency of tree species, 40 tree species belonging to 33 genera and 20 families were selected from 340 tree species widely used in Taiyuan City (Appendix Table S2). 40 tree species were classified into 32 tree species and 8 shrub species according to growth form, and 6 evergreen species and 34 deciduous species depending to life form.
In order to ensure the representativeness and facilitate observation and sampling, the selected sample site and distributed along the East Riverside Road. Meanwhile, the sample site and management conditions were basically consistent. Among the three selected tree species, each tree species met the conditions of good growth, similar age, thorax / ground diameter, plant height and crown width. Each sample site offered ,3 sample trees belonging to the same tree species. each tree species contained 9 sample trees selected from 3 sample sites. In total, 120 sample points (Fig. 5) and 360 sample trees were selected for 40 tree species.
5.3. Sampling and measurement
Green leaves and soil samples were collected during the middle July 2021. Senesced leaves samples were collected in November 2021. We gathered green leaves from the high, middle, and lower crowns of healthy trees (three combined into one). Each sample was composed of 3 sample trees from one sample site. First removed the litter layer (including undecomposed and semi-decomposed) to the exposed soil layer, then drilled the 0–30 cm soil layer with a soil drill. Like green leaves samples, samples of the soil and the senesced leaves were combined to create composite samples for each sample site. We collected 360 samples in total, including 120 green leaves samples, 120 senesced leaves samples and 120 soil samples.
The green and senesced leaves samples were first dried at 105 ◦C for 15 minutes before being dried at 65 ◦C to a constant weight. The dried materials were then crushed and put through a 100-mesh sieve. The soil samples were air dried, ground and gone through a 100-mesh sieve. The concentrations of total nitrogen and total phosphorus were measured with the colorimetric method. The process wa to add 5 mlH2SO4 and 6 mlH2O2 to the plants, and 1.85 g mixed catalyst and 5 mlH2SO4 to the soil. The samples were digested in a deboiling furnace, filtered at a constant volume, and then analyzed by automatic discontinuous chemical analyzer (Smartchem 450). The soil concentrations of NH4+-N, NO3−-N, NO2−-N and AP were also tested with the colorimetric method.
5.4 Date analysis
Taking into account the leaves mass loss when leaves senesce, we recalculated the senesced leaf nutrient concentrations to make up for the underestimating of NuRE using the mass loss correction factor (MLCF) [39] The MLCF values varied according to life forms: 0.745 for conifers, 0.780 for evergreen broadleaved plants, and 0.784 for deciduous broadleaved species [5]. In this research, all the data of Nusenesced had gone through quality correction. The calculated Nusenesced was also considered as nutrient utilization efficiency [6]. The NuRE could be quantified as follows:
Where Nugr represented the amount of nutrients in green leaves, while Nusen represented the amount of nutrients in senesced leaves.
Ngr, Pgr, Nsen, Psen, NRE, PRE and soil nutrient data were log10-transformed to achieve normalization. Analysis of variance (ANOVA) and the T-test with Bonferroni adjustments were used to examine for differences in the characteristics of nutrient absorption between different life forms. RDA was employed to examine the effects between two life forms. All data analyses were conducted in R 4.2.1.
Research involving plants. Experimental research and field studies on garden trees complied with relevant institutional guidelines and they were not collected from restricted area.
Data availability
The dataset generated during the current study is available from the corresponding author on reasonable request.
Acknowledgments
This work was financially supported by the Provincial Sci-Tech Promoting Program of Shanxi (2018YLCX32) and Postgraduate Innovation Project of Shanxi Province (2021Y343). We thank the Shanxi Agricultural University for providing this platform. Thank you for your suggestion.
Author contributions
R.Y.H. carried out the field sampling and laboratory work, did the statistical analyses and led the development of the manuscript. T.R.L. carried out the field sampling and revised the manuscript. R.R.Z. carried out the laboratory work. Y.X.Z. and J.P.G. revised the manuscript and gave final approval for publication. All authors have read and agreed to the published version of the manuscript.
Competing interests
The authors declare no competing interests.
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No competing interests reported.