Soil available phosphorus and moisture drive nutrient resorption patterns in plantations on the Loess Plateau

Forest Ecology and Management 461 (2020) 117910

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Soil available phosphorus and moisture drive nutrient resorption patterns in plantations on the Loess Plateau

T

⁎

Miaoping Xua,b, Zekun Zhonga,b, Ziyan Suna,b, Xinhui Hana,b, , Chengjie Rena,b, Gaihe Yanga,b a b

College of Agronomy, Northwest A&F University, Yangling 712100, China The Research Center of Recycle Agricultural Engineering and Technology of Shaanxi Province, Yangling 712100, China

A R T I C LE I N FO

A B S T R A C T

Keywords: Resorption strategies Plant growth Soil nutrient availability Soil water content Synergy effect Nutrient limitation

Nutrient resorption by senesced leaves is an important mechanism for the preservation of plant nutrients. However, our understanding of nutrient resorption patterns and drivers of plantations in Loess Plateau is limited. In this study, four main tree species (Robinia pseudoacacia [RP], Pinus tabuliformis [PT], Armeniaca sibirica [AS], and Caragana korshinskii [CK]) were compared in plantations on the Loess Plateau. We explored the relationships among nitrogen resorption efficiency (NRE), phosphorus resorption efficiency (PRE), plant nutrients (green leaf total nitrogen [TNgr] and total phosphorus [TPgr]), stand ages, growth rates (height growth rate [HGR] and diameter growth rate [DGR]), soil nutrients (soil total nitrogen [STN] and total phosphorus [STP]), available nutrients (soil inorganic nitrogen [SIN] and available phosphorus [SAP]), soil water content (SWC), and stoichiometries. We found that significant differences in nutrient resorption efficiencies among different afforested tree species. And the increase of N:P ratios of leaves and soil, and the decrease of SAP enhanced P-limited. Furthermore, the resorption efficiencies of different species differed in response to nutrients, stoichiometries, and plant growth. PRE was significantly negatively correlated with the DGR of deciduous species; however, NRE of N-fixing plant was positively correlated with plant growth rates. And the contributions of SWC and SAP were greater for nutrient resorption compared to other variables. The STN:STP and SIN:SAP were significantly correlated with leaf N:P, NRE, PRE, and PRE: NRE. Overall, plant growth rates may be regulated by absorption strategies due to leaf lifespan and N-fixing capacity of tree species. Resorption efficiencies were significantly correlated with SWC and SAP showed that soil moisture and available phosphorus were the primary drivers of nutrient resorption strategies. The association of PRE: NRE with N:P ratios indicated that nutrient resorption was driven by the coupling effect of N and P in plants and soil.

1. Introduction Nutrient resorption is the process by which nutrients (mainly nitrogen [N] and phosphorus [P]) are transferred from senesced leaves to storage organs or growing tissues (Killingbeck, 1996; Zhang et al., 2015c). This strategy is a key nutrient protection mechanism for plants and reduces the dependence of plants on soil nutrients (Deng et al., 2019; Hayes et al., 2014). The nutrient loss rate from senesced leaves is feedback from the plant to soil properties, whereas the nutrient concentration of litter affects the decomposition rate and soil nutrient supply (Tully et al., 2013; Yan et al., 2018). Therefore, understanding resorption strategies and their response factors are critical for exploring

the adaptive capacity of plants and nutrient cycling of plants and soils. As a major nutrient preservation mechanism, nutrient resorption efficiencies among different growth types are significantly different (Kobe et al., 2005; Vergutz et al., 2012). The data of nutrient resorption from American and European continental plant species have shown that the N resorption efficiency (NRE) of leaves of evergreen, deciduous, and herbaceous plants were 33–82%, 55–83%, and 28–78%, respectively, and P resorption efficiency (PRE) were 25–98%, 45–81%, and 34–92%, respectively (Aerts, 1996). Previous studies on different types of tree species in northern China have found that the NRE and PRE of macrophanerophytes were significantly higher than that of shrubs and that of evergreen trees were significantly higher than deciduous species

Abbreviations: NRE, nitrogen resorption efficiency; PRE, phosphorus resorption efficiency; TNsen, senesced leaf total nitrogen; TPsen, senesced leaf total phosphorus; TNgr, green leaf total nitrogen; TPgr, green leaf total phosphorus; STN, soil total nitrogen; STP, soil total phosphorus; SIN, soil inorganic nitrogen; SAP, soil available phosphorus; SWC, soil water content; RP, Robinia pseudoacacia; PT, Pinus tabuliformis; AS, Armeniaca sibirica; CK, Caragana korshinskii; PCA, Principal component analysis ⁎ Corresponding author at: College of Agronomy, Northwest A&F University, Yangling 712100, Shaanxi, China. E-mail address: [email protected] (X. Han). https://doi.org/10.1016/j.foreco.2020.117910 Received 9 December 2019; Received in revised form 12 January 2020; Accepted 14 January 2020 0378-1127/ © 2020 Elsevier B.V. All rights reserved.

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among different afforestation species; ii) plant growth rate is significantly correlated with nutrient resorption strategy; iii) soil nutrient availability and moisture may drive nutrient resorption patterns in senesced leaves. Therefore, the objectives of the study were to (i) describe the differences in leaf N and P resorption efficiencies, plant growth rates, and soil properties among different afforestation species; (ii) explore the main driving factors for leaf N and P resorption efficiencies in plantations on the Loess Plateau.

(Huang et al., 2007). Hence, the extension of plant leaf life enhances the nutrient utilization efficiencies of leaves (Lu et al., 2012). However, several studies have found that the resorption efficiencies were expressed as coniferous species > deciduous species > evergreen species (Vergutz et al., 2012). In addition, the NRE of N-fixing species was significantly lower than that of non-N-fixing species, whereas that for PRE was reversed (Barron et al., 2011; Inagaki et al., 2011). There were special cases where the PRE of a non-N-fixing plant (Banksia integrifolia) was much higher than that of an N-fixing plant (Acacia farnesiana) (de Campos et al., 2013). Therefore, it is important to explore the driving mechanisms to determine the differences in resorption efficiencies among different functional types of species. For long-lived species, there are differences in nutrient supply and resorption capacity at different ages (Mediavilla et al., 2014; Sun et al., 2016; Wang et al., 2014). In general, the resorption efficiencies of mature plants are higher than those of young plants, which is attributed to the increased nutrient demand of plant growth, thereby stimulating the nutrient preservation mechanism of leaves (Mediavilla and Escudero, 2004; Yan et al., 2018). Previous studies have revealed that the adaptability of plants to habitats gradually decreases with stand growth, resulting in a weakening of nutrient resorption (Deng et al., 2019; Hayes et al., 2014). Therefore, the relationship between nutrient resorption and age becomes more complicated. In addition, some studies found that the resorption of perennial herbaceous plants contributed significantly to the growth rates of plant height and reproductive organs (Ozbucak et al., 2011). However, other studies have shown that plant growth is not associated with nutrient resorption (Pasche et al., 2002). Thus, whether nutrient resorption affects plant growth requires further evaluation. Nutrient resorption is closely related to the availability of soil nutrients (Zheng et al., 2018; Zhou et al., 2016). For example, nutrient resorption efficiencies have been shown to decrease with increasing soil nutrient availability (Lu et al., 2012). Studies have found that the NRE of leaves was driven by soil inorganic N (SIN) (Huang et al., 2018). The limitations of soil available P may affect nutrient loss rates of senesced leaves (Tully et al., 2013). Moreover, plant acquisition strategies for soil P are related to the intrinsic traits of species (Tully et al., 2013; Wang et al., 2014). Previous studies have shown that nutrient resorption increased (Diehl et al., 2003), decreased (Kobe et al., 2005), or was neutral (Du et al., 2017) with changes in leaf N and P concentrations. Further, plant and soil nutrient concentrations are significantly correlative (Zhang et al., 2019). Soil moisture is critical in the regulation of soil nutrient availability (Lue and Han, 2010). However, the potential response mechanism of nutrient resorption strategies to soil nutrient availability remains unclear. Although major breakthroughs have been made in the study of resorption strategies (Drenovsky et al., 2019; Yuan et al., 2018; Zhang et al., 2015b), how N:P ratios of plants and soil in ecosystems regulate resorption efficiencies remains unresolved. Previous studies have found significant correlations between plant and soil N:P ratios (Fan et al., 2015; Zhang et al., 2019; Zhong et al., 2019). Many existing studies have focused on one-sided examinations of NRE and PRE, yet there is little awareness of antagonism synergies between the two. Plantations have significantly improved soil nutrients and P is the main limiting nutrient on the Loess Plateau (Liu et al., 2018a; Ren et al., 2016). Simultaneously, the low soil moisture restricts plant growth and nutrient utilization efficiency on the Loess Plateau (Zhang et al., 2019). Therefore, understanding N and P concentrations and their ratios in plants and soil is critical for determining the driving mechanism of resorption efficiencies. Here, we studied leaf nutrient resorption efficiencies at different ages for different afforestation species (Robinia pseudoacacia, Pinus tabuliformis, Armeniaca sibirica, and Caragana korshinskii) and linked N and P resorption strategies to plant nutrients, growth rates, soil nutrients, available nutrients, and stoichiometries. We tested the following hypotheses: i) nutrient resorption patterns differ significantly

2. Material and methods 2.1. Study area and species This study was conducted at a plantation area in the Wuliwan catchment (36°51′13″–36°52′18″ N, 109°20′53″-109°21′27″ E, average elevation 1290 m) in the northern Shaanxi province, China, which has a semiarid climate. The average annual temperature is 8.8 °C and the average annual precipitation is 510 mm, of which 65%–75% is distributed during the plant growing season from May to September (Zhang et al., 2018a). There are 2415 h of sunshine and a frost-free period of 157 days per year (Ren et al., 2017). Before the production of plantations, the original crop was maize. The fertilizing regimes before afforestation were the same, i.e., 50 kg ha−1 year−1 urea and 25 kg ha−1 year-1P pentoxide, but this was stopped when afforestation commenced (Zhang et al., 2018a). We studied and investigated four major plantations in this area, grouped in four growth types: deciduous macrophanerophytes (Robinia pseudoacacia, RP), evergreen conifers (Pinus tabuliformis, PT), deciduous dungarunga (Armeniaca sibirica, AS), and deciduous shrubs (Caragana korshinskii, CK). We identified which species were N-fixing (RP and CK) and non-N-fixing (PT and AS). The soil properties (including soil nutrients, aggregate structure, water conservation function, etc.) have been greatly improved after afforestation in the area (Li et al., 2019; Liu et al., 2018a; Zhang et al., 2018b, 2019). The four typical vegetation types (RP, PT, AS, and CK) restored in four age groups (13, 19, 29, and 44 years) were selected as the experimental sites. Among these, only PT was an evergreen conifers and the other tree species were deciduous. The average heights and diameter at breast height (DBH) of all examined tree species were presented as RP > PT > AS > CK. All selected lands were located at similar altitudes, gradients, and slopes, and had similar farming practices prior to afforestation (Table S1). 2.2. Plant and soil sampling Three replicate plots (20 × 20 m2) were randomly placed at each independent replicate site for subsequent investigation and sampling. For the number of species in each plot, the height and DBH of trees were measured using a height gauge and tapeline, respectively. The average height growth rate (HGR) and diameter growth rate (DGR) were calculated by dividing the height and DBH by stand ages (Zhang et al., 2015a). For each age class of plant, green and senesced leaves were collected from five representative trees of similar heights and DBH within each plot. Green leaves were sampled from the lower and middle outer canopies and pooled for each marked tree in July 2018. To avoid nutrient decomposition and leaching, senesced leaves were collected by gently shaking the branches from the original marked trees from July to October 2018. All leaf samples were taken to the laboratory immediately after collection and washed with deionized water. These were oven-dried at 105 °C for 10 min and then at 75 °C for 24 h to a constant weight and sieved with a 0.1 mm sieve. Soil samples were collected (topsoil, 0–10 cm) when sampling plant leaves. After removing the litter layer and other debris, soil samples were taken from 10 points in an “S” shape using a soil auger (5 cm in diameter). The soil samples were homogenized to produce a final soil sample. All soil samples were quickly sieved with a 2 mm mesh. The soil samples were air-dried and stored at room temperature (25–30 °C) to 2

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3.2. Factors affecting nutrient resorption

assess the soil properties.

Leaf nutrients, stoichiometries, and growth rates also varied widely among the different species (Table S2). Soil nutrients (STN and STP), available nutrients (SIN and SAP), stoichiometries, and SWC were significantly different among species, and these soil properties increased significantly with stand ages within each species (apart from the SAP of RP and CK that was significantly decreased) (Fig. S1). Notably, the comprehensive analysis of nutrient resorption efficiency of all tree species found that the contribution of plant species, growth rates, stand ages and leaf nutrients, soil nutrients and moisture could explain 82.1% of nutrient resorption efficiency (Fig. 2), with soil nutrients presenting the maximum effect. In addition, the contributions of SAP and SWC to nutrient resorption efficiencies were 21.2 and 16.0%, respectively. The responses of NRE, PRE, and their ratio to stand ages and growth rates were significantly different among the four tree species (Figs. 3 and 4). The NRE of N2-fixing tree species (CK) and deciduous tree species (AS) were negatively correlated with stand ages, but positively correlated with HGR and DGR, whereas the PRE were reversed. The NRE and PRE of PT were significantly positively correlated with stand ages and HGR. The PRE of RP was significantly positively correlated with stand ages and negatively correlated with plant growth rates. In addition, except for PT, the leaf PRE: NRE ratios of other three tree species increased significantly with stand ages. Correlation analysis showed that nutrient resorption efficiencies were closely related to soil nutrients and moisture (Fig. 5). The STN and SIN were significantly negatively correlated with NRE and significantly positively correlated with PRE, which may be related to N- cycle in plants and soil, except for leaf NRE of PT. The STP was significantly positively related to PRE. On the one hand, SAP was positively correlated with NRE. On the other hand, SAP was negatively correlated with PRE of RP and CK and positively correlated with PRE of PT and AS. These results may be closely related to P- limited in the area. The SWC was significantly negatively correlated with NRE of RP and AS, and positively correlated with the PRE of PT and CK. The correlation analysis of the stoichiometry showed that the PRE: NRE ratio of AS and CK was significantly positively correlated with soil STN: STP, but that was negatively correlated with leaf TN: TPgr (Fig. 6). And the PRE: NRE ratio of RP, AS and CK was positively correlated with TN:TPsen and SIN:SAP ratio.

2.3. Analysis of leaf and soil properties Total N (TN) of the plants and soil was determined using the Kjeldahl method (Mulvaney et al., 1992). After wet digestion with HClO4-H2SO4, total P (TP) was determined by colorimetry (Ren et al., 2016). Ammonia N (NH4+-N) and nitrate N (NO3–-N) of the soil were measured using an AA3 continuous flow analysis system (SEAL, Germany) and 1 mol L-1 KCl extraction. SIN is the sum of NH4+-N and NO3– -N concentration and is expressed in mg kg−1 soil (Wang et al., 2014). Soil available P (SAP) was measured using a spectrophotometer (Mapada Corporation, China) with a 0.5 mol L−1 NaHCO3 extraction (Olsen and Sommers, 1982). Soil water content (SWC) was determined by oven drying the sample at 105 °C to a constant mass (Zhao et al., 2015). 2.4. Calculation of resorption efficiency Nutrient resorption efficiency can be expressed in terms of the mass basis or leaf area basis. The leaf area of senesced leaves may be atrophied or folded underestimated (See et al., 2015). The concentrations of TN and TP in green and senesced leaves were used to calculate the nutrient resorption efficiencies (Killingbeck, 1996):

REnutrient =

[nutrient] gr − [nutrient] sen × 100% [nutrient] gr

(1)

where, REnutrient is the nutrient resorption efficiency; [nutrient]gr is the nutrient concentration in the green leaves; and [nutrient]sen is the nutrient concentration in the senesced leaves. 2.5. Statistical analyses The Shapiro–Wilk test was used to check the distribution of all data and all variables followed a normal distribution. Statistical analyses of the data were performed using SPSS (Version 20; SPSS Inc., Chicago, IL, USA). Differences in nutrient concentrations, stoichiometry, tree height, DBH growth rates, and nutrient resorption efficiencies of different species and stand ages were determined by two-way analysis of variance (ANOVA). Principal component analysis (PCA) was used to evaluate the overall differences in nutrients and resorption of senesced leaves among the different species. Redundancy analysis was used to identify the effects of stand ages, and plant growth rates, plant and soil nutrients and soil moisture on leaf nutrient resorption efficiency. Multivariate linear regressions were used to test the correlations among stand ages, growth rates, SWC, soil nutrients, and soil available nutrients, nutrient resorption efficiencies, and their stoichiometries of four different species. Pearson correlation analysis were used to analyze the relationships among leaf nutrients, resorption efficiencies, soil nutrients, available nutrients and stoichiometries, SWC, and plant growth rates.

4. Discussion 4.1. Nutrient resorption efficiencies among different afforested species and stand ages We hypothesized that the nutrient resorption patterns of leaves were different among different plantations. We found that the nutrient resorption efficiency of evergreen conifers (PT) was significantly higher than that of deciduous plants (Table 1). This finding was consistent with the conclusion of Huang et al. (2007) that the surface area of needle-like leaves for conifers is small and the oily layer on the surface of the leaves slowed the transport rate of organic matter. Kimmins (1976) reported that the prolongation of plant leaf lifespan promoted the transfer of nutrients from green leaves to senesced leaves, which enhanced their viability in low temperature environments. Moreover, the time that leaves remain on the plant body increases, forcing the cost of maintaining plant growth and photosynthesis to increase, resulting in increased nutrient use efficiencies (Aerts and Chapin, 2000). In addition, PCA determined significant differences in resorption efficiencies between species of different functional types (Fig. 1). And Vergutz et al. (2012) found that the resorption efficiency of macrophanerophytes was greater than that of shrubs by integrating 86 resorption studies worldwide. We found that the senesced leaves of CK and AS had lower nutrients than the other species (Table S2). Therefore, the macrophanerophytes absorbed nutrients through the absorption of senesced

3. Results 3.1. Nutrient resorption The four tree species showed large differences in NRE and PRE as well as PRE:NRE ratio (Table 1). The NRE of RP, PT, and AS was higher than that of CK by 22.07%, 55.59%, and 44.44%, respectively. The PRE of RP, PT, and CK was higher than that of AS by 27.54%, 35.21%, and 4.21%, respectively. PCA was used to assess the overall difference in nutrients and resorption efficiencies of senesced leaves among the different species (Fig. 1). The two PCA axes explained the total variations of 58.87% and 22.41%, respectively. We found that the resorption efficiencies were significantly different among different species. 3

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Table 1 Intra- and interspecific differences in nutrient resorption efficiencies of leaf among four different species groups. Values ± SE Species NRE (%) RP PT AS CK PRE (%) RP PT AS CK PRE:NRE ratio RP PT AS CK

13 years

19 years

29 years

44 years

Intraspecific age difference

Interspecific species difference

P-value

P-value

48.20 56.94 59.40 43.63

± ± ± ±

1.73Bb 0.42Ab 0.22A 4.03Ba

50.07 59.03 57.22 41.50

± ± ± ±

0.93Bab 0.75Ab 2.09A 2.96Cab

53.99 64.47 54.82 39.36

± ± ± ±

1.01Ba 1.41Aa 0.37B 0.75Cab

41.80 66.88 53.35 34.45

± ± ± ±

0.99Cc 2.67Aa 4.02B 0.78Cb

0.001 0.007 0.319 0.147

< 0.001

45.20 43.35 31.26 32.67

± ± ± ±

0.43Ab 0.70Ac 1.96Bc 1.10Bd

45.94 49.20 34.81 36.32

± ± ± ±

0.76Ab 0.70Ab 2.02Bbc 0.37Bc

47.12 52.31 38.86 39.98

± ± ± ±

0.28Bab 1.80Aab 1.85Cab 1.77Cb

49.39 54.05 42.21 44.37

± ± ± ±

1.43Ba 2.11Aa 0.83Ca 0.41Ca

0.036 0.004 0.010 < 0.001

< 0.001

0.002 0.443 0.010 < 0.001

< 0.001

0.94 0.76 0.53 0.76

± ± ± ±

0.04Ab 0.0B1 0.03Cc 0.06Bc

0.92 0.83 0.61 0.88

± ± ± ±

0.02bA 0.02A 0.06Bbc 0.06Ab

0.87 0.81 0.71 1.01

± ± ± ±

0.01Bb 0.02B 0.03Cab 0.03Ab

1.18 0.81 0.80 1.29

± ± ± ±

0.06Aa 0.05B 0.04Ba 0.03Aa

Site codes: F-value and P-values are from paired t-tests. NRE means nitrogen resorption efficiency, PRE means phosphorus resorption efficiency. Different capital letters show significant differences among tree species at p < 0.05. Different lowercase letters represent significant differences among ages at p < 0.05. RP: Robinia pseudoacacia, PT: Pinus tabuliformis, AS: Armeniaca sibirica, CK: Caragana korshinskii.

Fig. 2. Effects of stand ages, and plant growth rates, plant and soil nutrients and soil moisture on leaf nutrient resorption efficiency. TNgr: green leaf total nitrogen, TPgr: green leaf total phosphorus, STN: soil total nitrogen, STP: soil total phosphorus, SIN: soil inorganic nitrogen, SAP: soil available phosphorus, SWC: soil water content. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.) Fig. 1. Principal component analysis (PCA) was used to evaluate the overall differences in nutrients and resorption of senesced leaves among different species. NRE: nitrogen resorption efficiency, PRE: phosphorus resorption efficiency, TNsen: senesced leaf total nitrogen, TPsen: senesced leaf total phosphorus. RP: Robinia pseudoacacia, PT: Pinus tabuliformis, AS: Armeniaca sibirica, CK: Caragana korshinskii.

and absorption capacity are significantly different at different ages, which affects the resorption strategy of senesced leaves (Wang et al., 2014). We found that the resorption efficiencies of PT and the PRE of the other three species increased with stand ages (Fig. 3a and b), which was similar to the results of previous studies that found that old or mature plants had higher resorption efficiencies than younger ones (Aerts and Chapin, 2000; Huang et al., 2007). Soil P is relatively low in the studied region compared to global levels and its ability to obtain available P is limited due to water scarcity (Li et al., 2007). Notably, we found that PRE:NRE ratio increased significantly with stand ages (Fig. 3c), which may be associated with P-limited in this area. The growth rate hypothesis emphasizes that the growth of most microbes is related to the need for P for ribosomal RNA synthesis (Ren et al., 2016; Xu et al., 2019). The P-limited promoted weakening of microbial metabolism, thereby slowing absorption of soil available nutrients by plants (Liu et al., 2018a; Zhang et al., 2018b). Plant growth is accompanied by the slowing of the efficiency of organs and tissues that

leaves, rather than absorbing nutrients through green leaves, but this was reversed for the shrubs (Zhang et al., 2015c). Considering the biological N2-fixation capacity of plants, we found that the NRE of Nfixing plants (RP and CK) was significantly lower than that of non-Nfixing plants (Table 1). The root nodule of N-fixing trees is associated with microbes and can convert N into plant-available forms that are common in ecosystems (Barron et al., 2011; Tully et al., 2013). Therefore, the stronger biological N-fixation capacity promoted an intake of N by N-fixing plants, which reduced the transfer of nutrients in senesced leaves. Our results showed that the plant’s own lifespan had a significant effect on leaf resorption (Fig. 3). For long-lived species, nutrient supply 4

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Fig. 3. Relationship of stand ages with N and P resorption efficiencies and PRE:NRE ratio among tree species with different functional types. RP: Robinia pseudoacacia, PT: Pinus tabuliformis, AS: Armeniaca sibirica, CK: Caragana korshinskii. *P < 0.05, **P < 0.01.

Fig. 4. Relationship of height and diameter growth rates with N and P resorption efficiencies and PRE:NRE ratio among tree species with different functional types. RP: Robinia pseudoacacia, PT: Pinus tabuliformis, AS: Armeniaca sibirica, CK: Caragana korshinskii. *P < 0.05, **P < 0.01.

in this area (Ren et al., 2016; Zhang et al., 2019). Furthermore, the relatively high senesced leaf N: P indicated that more P was resorbed than N. Therefore, we expected that P-limited increased phosphorus resorption in senesced leaves. And our results showed that soil available phosphorus and moisture were the main drivers for nutrient resorption (Fig. 2). In semi-arid regions, soil moisture limitation is an important factor restricting plant growth and nutrient uptake (Zhao et al., 2018). In addition, the utilization efficiency of soil nutrient by plants is closely related to plant growth rate (Tully et al., 2013). Simultaneously, we found that the high growth rate of plant significantly affected nutrient resorption (Figs. 2 and 4). Thus, plant growth rates may indirectly drive leaf nutrient resorption strategies. We found that height and DBH growth rates of RP, AS, and CK were

transport nutrients, thereby stimulating the nutrient resorption efficiencies of senesced leaves to decrease nutrient loss, which contributes to plant adaptation and survival (Vergutz et al., 2012). In addition, the NRE of CK and AS decreased with stand age (Fig. 3a). The reasons for this may be the adaptability of plants to habitats gradually decreased with age and a decline in nutrient preservation occurred, which directly led to the weakening of resorption (Yan et al., 2018; Yuan and Chen, 2010). 4.2. Association of nutrient resorption efficiency with factors in plants and soil Phosphorus appears to be the main limiting nutrient for plantations 5

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Fig. 5. Leaf N and P resorption efficiency in relation to soil nutrients, available nutrients and soil water content among tree species. RP: Robinia pseudoacacia, PT: Pinus tabuliformis, AS: Armeniaca sibirica, CK: Caragana korshinskii. *P < 0.05, **P < 0.01.

photosynthetic reactions were closely related to the plant growth rate, thereby affecting the resorption of N by senesced leaves (Zhang et al., 2015b). In addition, the plant’s own efficiency in synthesizing proteins and nucleic acids is reduced as the plant ages, reducing the plant growth rate, and thereby stimulating the resorption strategies of senesced leaves for plant growth. We found that the leaf PRE:NRE ratio was significantly negatively correlated with the growth rate of deciduous species (Fig. 4). The decrease of soil available P slowed the transport of P by plant phloem, which affected the synthesis of plant

significantly negatively correlated with PRE and positively correlated with NRE (Fig. 4). This result was consistent with the conclusions of Zhang et al.’s (2015a) study on the effects of plant growth rates on resorption efficiencies. Changes in the NRE of these plants were associated with the N fixation of the species (Huang et al., 2007; Lu et al., 2012). Several studies have shown that the resorption of N by senesced leaves can provide most of the N for plant growth (Barron et al., 2011; Killingbeck, 1996). The concentration of leaf N was significantly correlated with growth rate (Table S3), indicating that N-related

Fig. 6. Relationship of height and diameter growth rate with N and P resorption efficiencies of leaves with functional tree species. RP: Robinia pseudoacacia, PT: Pinus tabuliformis, AS: Armeniaca sibirica, CK: Caragana korshinskii. *P < 0.05, **P < 0.01. 6

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limitation may be a long-term nutrient balance constraint in this region (Liu et al., 2018a; Zhang et al., 2019). As plants grow, the N:P ratio of senesced leaves was higher than that of green leaves (Table S2). Simultaneously, we found that the N:P ratio of senesced leaves was significantly higher than that of non-N-fixing trees. The differences in leaf nutrients were synchronized with NRE and PRE (Table 1, Table S3). Therefore, P resorption of senesced leaves was higher than that of N. Strong phosphatase activity has been found in the soils of N-fixing species in temperate regions (Tully et al., 2013). Similarly, the restriction of soil P regulates the absorption of N by plant roots (Fan and Guo, 2010; Schreeg et al., 2014). These results indicate that there were mutual driving effects between N and P of plants and soil. Therefore, the leaf PRE:NRE ratio was driven synchronously by the N and P of plants and soils among different afforestation species.

growth substances (e.g., nucleic acids and proteins) (Renteria and Jaramillo, 2011; Zhang et al., 2015a). As perennial plants grow, a series of processes affect the allocation and utilization of resources (Vergutz et al., 2012). As the growth of the trunk increases, more biomass is distributed to the stem and nutrient distribution is transferred from the leaves to woody tissue (Stephenson et al., 2014). This change in biomass and energy distribution will ultimately change the nutrient requirements and affect nutrient resorption. We hypothesized that the changes in soil nutrient availability drive the dynamics of leaf nutrient resorption strategies. NRE and PRE were significantly affected by SIN and SAP (Fig. 5 and Table S3). We also found that soil SIN and SAP were significantly correlated with leaf N and P (Table S3), which may have affected leaf resorption strategies (Hagen-Thorn et al., 2006; Vourlitis et al., 2014). The results showed a significantly negative correlation between NRE and SIN in RP and CK (Fig. 5c). This was consistent with the nutritional absorption conclusions of Kobe et al. (2005) that were shown to decrease as the supply of soil available nutrients increased. Several studies have shown that Nfixing species promote N mineralization and absorption, which in turn increase N efficiency (Chavez-Vergara et al., 2015; Ren et al., 2017). Therefore, as the effectiveness of soil N increases, senesced leaves decrease the resorption efficiency of N. We found that soil available P was significantly positively correlated with NRE and negatively correlated with PRE (Fig. 5). PRE increased significantly with stand age (Table 1). Our previous studies showed that plantation growth strengthened soil P, which was limited in this area (Zhang et al., 2019; Zhao et al., 2017). Soil P is relatively low in areas with poor soils and water constrains the supply of P (Almeida et al., 2019; Mei et al., 2019). P limitation significantly reduces the utilization strategy by the plant for soil P, leading to increased PRE via metabolically unstable inorganic P components before detachment (Drenovsky et al., 2019; Lu et al., 2019). Therefore, the availability of soil nutrients can have negative effects on the nutrient resorption efficiency. However, due to the lack of research on P conversion in plant vascular systems, this conclusion was not in-depth and requires further research. Our study showed that soil STN:STP and SIN:SAP significantly affected leaf nutrient resorption efficiencies and TN:TPsen (Table S3). This result implied that soil nitrogen and phosphorus may respond synergistically, thus affecting the resorption of leaf N and P. On the one hand, the significant increase in the ratios of STN:STP and SIN:SAP was manifested by a significant decrease in SAP (Fig. S1), suggesting P limitation of the soil (Liu et al., 2018a; 2018b; Zhao et al., 2018). On the other hand, the synthesis of RNA in plants is regulated by P, which indirectly affects the N turnover of plants (Ren et al., 2017; 2016). Notably, several studies have shown that P limitation alters the preservation and resorption of N by plants (Tully et al., 2013; Yuan et al., 2018; Lu et al., 2012).We found that soil STN:STP and SIN:SAP ratios were significantly correlated with the plant leaf TN:TPsen ratio (Table S3). This result was consistent with the results by Zhang et al. (2019) that plants and soils have a synergistic response to N and P. Furthermore, our results showed that soil moisture was significantly correlated with leaf nutrient resorption efficiencies and soil nutrients (Table S3 and Table S4). The ability of plantations to fix water increases soil moisture, which is a crucial factor affecting the microbial activity and substrate decomposition (Liu et al., 2018b; Ren et al., 2016). In general, an increase in soil moisture enhances the leaching of soil nutrients and the utilization of available nutrients by soil microorganisms, which significantly affects soil available nutrients (Wang et al., 2009; Zhang et al., 2018a). Overall, Soil moisture and available phosphorus were the primary drivers of nutrient resorption strategies.

5. Conclusion In summary, the evidence indicated that the leaf life span and Nfixation capacity of tree species have significant effects on nutrient resorption strategies in the present study. There were significant correlations between plant growth rates and nutrient resorption efficiencies, indicating that plant growth rates were highly likely to be controlled by the resorption strategies of N and P in senesced leaves. Resorption efficiencies were significantly correlated with SWC and SAP showed that soil moisture and available phosphorus were the primary drivers of nutrient resorption strategies. Furthermore, the leaf PRE:NRE ratio was closely related to the N:P ratio of plants and soil, suggesting that nutrient resorption efficiency of senesced leaves was driven synchronously by the N and P in plants and soil. CRediT authorship contribution statement Miaoping Xu: Conceptualization, Methodology, Software, Data curation, Writing - review & editing. Zekun Zhong: Visualization, Investigation. Ziyan Sun: Visualization, Investigation. Xinhui Han: Conceptualization, Methodology, Software. Chengjie Ren: Software, Validation. Gaihe Yang: Supervision. Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgments The authors greatly appreciate the assistance of Wenli Wu and Xing Wang (Northwest A & F University, China) in conducting experiments. National Natural Science Foundation of China (No. 41877543) financially supported this work. The authors are also grateful to anonymous reviewers whose comments and suggestion helped us to enhance the quality of this paper. Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.foreco.2020.117910. References Aerts, R., 1996. Nutrient resorption from senescing leaves of perennials: are there general patterns? J. Ecol. 84, 597–608. Aerts, R., Chapin, F.S., 2000. The mineral nutrition of wild plants revisited: A re-evaluation of processes and patterns. In: Fitter, A.H., Raffaelli, D.G. (Eds.), Advances in Ecological Research, Vol. 30, pp. 1–67. Almeida, J.P., Rosenstock, N.P., Forsmark, B., Bergh, J., Wallander, H., 2019. Ectomycorrhizal community composition and function in a spruce forest

4.3. Response of nutrient resorption to nutrient stoichiometry in plants and soil We found that the leaf PRE:NRE ratio was significantly correlated with leaf N:P, soil STN:STP, and SIN:SAP ratios (Fig. 6 and Table S3). P 7

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