Replanting of broadleaved trees alters internal nutrient cycles of native and exotic pines in subtropical plantations of China

Yong Lin,Chengkng Xi,Goyng Wu,Fngho Wng,Shengnn Wng,

Yuanqiu Liua,d,Fusheng Chena,d,＊

a Key Laboratory of National Forestry and Grassland Administration on Forest Ecosystem Protection and Restoration of Poyang Lake Watershed,Jiangxi Agricultural University,Nanchang,330045,China

b Jiangxi Forestry Resources Monitoring Center,Nanchang,330045,China

c Postdoctoral Research Station of Management Science and Engineering,Nanchang University,Nanchang,330031,China

d Jiangxi Provincial Key Laboratory of Silviculture,College of Forestry,Jiangxi Agricultural University,Nanchang,330045,China

Keywords:Interspecific interaction Mixture effect Needle resorption N and P translocation Root capture

A B S T R A C T Background:The replanting of broadleaved trees in pure coniferous plantations is widely implemented,as mixed plantations are generally more stable and functional.However,the effect of interspecific interactions between broadleaved and coniferous trees on internal nutrient cycles of conifers remains unclear.

1.Introduction

Forest plantations are the main contributor to increasing the global forest area(FAO,2020).The area of plantations in China(69.33 million ha)ranks first in the world,accounting for one-third of global plantations(FAO,2020;Liu et al.,2021).These plantations with single tree species,especially coniferous species,often have detrimental consequences on soil sustainable fertility and nutrient cycling during forest development(Liu et al.,2018).The replanting of broadleaved trees in pure coniferous plantations is an effective and common forest management method to enhance resource-use efficiency(Hoogmoed,2014)and stimulate nutrient cycling by mobilizing immobile soil nutrients and increasing plant uptake(Maxwell et al.,2020;Li et al.,2021).Strikingly,the interaction between broadleaved and coniferous species could alter the nutrient acquisition strategies of conifers and could affect their nutrient cycling(Yan et al.,2019).For example,Bu et al.(2020)found that mixed broadleaved trees increased soil nutrients but decreased the coniferous tree nutrient content.However,it remains uncertain how interspecific interactions affect the nutrient cycles of conifers in mixed plantations.

The process of internal nutrient cycling in trees includes nutrient acquisition(root capture and leaf resorption)and translocation(Kobe et al.,2005;Wu et al.,2021).Root capture(from the soil to roots)is often considered a belowground nutrient acquisition strategy that is initially achieved by absorptive roots(Kou et al.,2017).Previous studies have indicated that root nutrient capture is affected by neighboring species(Simon et al.,2014),but the results on the magnitude and direction remain controversial(Hong et al.,2017;Liu et al.,2021).Leaf resorption is an important aboveground nutrient conservation strategy that reallocates nutrients from senesced tissues to other functionally active tissues(Aerts,1996).Additionally,nutrient translocation is a key mechanism to reduce nutrient loss because plants translocate limiting nutrients to the growing apex(Aldous,2002).In recent decade,the responses of plant nutrient acquisition strategies to changing environments have been widely concerned(Sardans et al.,2017;Wu et al.,2021;Song et al.,2022),but the impact of neighboring species on the nutrient cycling process within the target trees has not been effectively evaluated.

Each process demands distinct levels of resource investments,as well as its own potential consequences for internal nutrient cycles of trees.Previous work has shown that a trade-off often exists between capture and resorption strategies(Kou et al.,2017;Wu et al.,2021),and emphasized that the allocation of resources toward nutrient capture and resorption depends on both the soil nutrient availability and the cost involved in these processes(Wright and Westoby,2003;Wang et al.,2014).For instance,plants preferentially employ a capture strategy in nutrient-rich environments due to the relatively lower cost of exploiting nutrients in nutrient-rich soils(Hayes et al.,2014;Huang et al.,2015).Recent evidence suggest that soil nutrients alone may not adequately predict the nutrient acquisition patterns of plants(Tully et al.,2013;Liu et al.,2021).In mixed plantations,the energetic cost of nutrient uptake by roots increases under the competition of belowground nutrients among species(Liu et al.,2021),thus plants may adopt the resorption strategy rather than the capture strategy.Therefore,it is necessary to know whether and how replanting broadleaved trees affect the nutrient acquisition strategy of coniferous trees with the increasing conversion from pure plantations to mixed forests.

Pinus massoniana(native pine)andP.elliottii(exotic pine)are the most frequently used coniferous species for afforestation in southern China,with a total coverage of 10.01 and 2 million ha,respectively(Chen et al.,2019).In the past 10 years,the replanting of broadleaved trees has been widely implemented in pure plantations to improve plantation structure and enhance the resistance of pines to disease and pests(Li et al.,2021).Interestingly,these two pine species have different adaptive traits to replanted broadleaved trees.In a field investigation,we found that the growth rate of native pine was lower than that of exotic pine in middle-aged and near-mature mixed plantations with broadleaved trees,but the opposite pattern was observed in pure plantations.Similarly,Yan et al.(2019)reported that mixed broadleaved trees increased the total root length of native pine and decreased the ectomycorrhizal colonization rate,which is contrary to the response of exotic pine.Therefore,interspecific interactions may affect the nutrient acquisition and utilization strategies of trees(Yan et al.,2019;Liu et al.,2021),which help to explain the effects of neighboring species on the growth of target trees.

Nitrogen(N)and phosphorus(P)are generally considered the two most essential and limiting elements for tree growth and nutrient cycling in terrestrial ecosystems(Chen et al.,2015a).The low availability of N and P in plantations soil in subtropical China is due to deforestation and logging(Bu et al.,2020),coupled with high rainfall in this region exacerbating N and P losses through leaching and erosion.In this context,it is critical to understand how conifers in mixed plantations adjust internal nutrient cycling to alleviate N and P deficiencies.Here,our long-term field experiment provides an ideal platform to study the effects of interspecific interactions between pine and broadleaved trees on internal nutrient cycles of native and exotic pines.We hypothesized that(1)the input of leaf litter from broadleaved trees would improve soil nutrients,thereby increasing the N and P contents of pine tissues in mixed plantations.(2)The interspecific interactions between pine and broadleaved trees might have a negative effect on belowground nutrient capture of native pine and a positive effect on exotic pine based on the divergent adaptive traits of the two pine species.(3)Native pine would be more inclined to employ the aboveground nutrient resorption strategy in response to mixed planting as compared to exotic pine,according to the“capture and resorption trade-off”theory(Wright and Westoby,2003).

Fig.1.Experimental design of tree spacing and soil blocks collection under crown.

2.Materials and methods

2.1.Study site and experimental design

This study was conducted in the Forest Vegetation Restoration region(26°44′N,115°04′E)of Degraded Red Soil in Taihe County,Jiangxi Province,China.The area of this field is approximately 133 ha,with an altitude of 70–130 m above sea level.The site is characterized as a subtropical monsoon climate with a warm,wet summer and a cool,dry winter.The mean annual precipitation and temperature are approximately 1,600 mm and 18.6°C,respectively.The stands are located on highly weathered and degraded Ultisol(locally called‘red soil’)that is predominantly clay-like with a high bulk density,low organic matter content and low porosity(Wang et al.,2019).

The zonal vegetation in this area is evergreen broadleaved forest,but it was extremely degraded,forming shrubs,before 1990 due to frequent human disturbance,such as logging and firewood collection(Wang et al.,2007).In 1991,the seedlings of native pine and exotic pine were planted at a spacing of 3 m×3 m after shrub clearing and soil preparation.To evaluate the potential effect of stand transformation from pure to mixed plantations,approximately 1/3 of the pure plantations of native and exotic pines were moderately thinned and planted with a broadleaved species(2-year-old seedlings ofSchima superba)in 2006.The ratio of pine toS.superbawas approximately 1:1 in the mixed plantations.Thus,each of the pine pure plantations(native pine and exotic pine)and mixed plantations(mixed withS.superba)was independently and randomly distributed on 5 different hills(20 hills in total)in the study area(Fig.S1).

In July 2017,we designed a complete randomized experiment with 5 replicates of 4 treatments(native pine in pure plantation-NP,exotic pine in pure plantation-EP,native pine in mixed plantation-NM and exotic pine in mixed plantation-EM)in order to identify the differences of internal nutrient cycles among native and exotic pines in pure and mixed plantations.Specifically,a 20 m×20 m plot was established in each of 20 different hills,and all of these plots have approximately the same slope angle(8%–10%).Five plots distributed in different hills of eachforest types(NP,EP,NM and EM)were investigated(Fig.S1)and obtained the stand characteristics in this study(Table S1).

Table 1Nutrients in rhizosphere soil and different tissues of native and exotic pines in pure and mixed plantations in subtropical China.

2.2.Sample collection

In each plot,six pine trees were selected based on the average diameter at breast height and height(Table S1)to collect rhizosphere soils,fine roots,twigs and needles.Specifically,we sampled a total of four soil blocks(20 cm in length,20 cm in width and 10 cm in depth;24 blocks were collected in each plot)from the southern to northern transect under the crowns of each treeat50 and 100cm fromthe treetrunk(Fig.1),and carefully removedthe intact fine root systems(<2 mm in diameter).The soil that adhered to the surface(<4 mm)of fine roots after hand-shaking was considered rhizosphere soil(Phillips and Fahey,2008).The rhizosphere soil samples of each plot were completely mixed into a composite sample,stored at 4°C and transported to the laboratory immediately for the determination of available nutrients(NH4+-N,NO3--N and available phosphorus).The fine roots were further divided into absorptive(1–2 order roots)and transport(3–5 order roots)roots(Chen et al.,2015b;Kou et al.,2017).The fine root biomass and specific root length of the absorptive and transport roots of each soil block were measured after washing with ultrapure water.Finally,the absorptive and transport roots of the pines in the 24 soil blocks per plot were mixed into a composite sample and ground to pass through a 0.15-mm sieve prior to chemical analysis.

In addition,the twigs and mature needles were collected from the upper two-thirds of representative tree crowns in multiple directions by using a tree trimmer.Moreover,five 1 m×1 m senesced needle traps were set randomly in each plot.Similarly,we used the above method to form a composite sample for twigs and mature and senesced needle samples of each plot.These samples were also oven-dried to a constant weight(65°C for 72 h)and ground to pass through a 0.15-mm sieve for nutrient analysis.

2.3.Chemical analysis

The soil moisture content was determined using 10-g subsamples.Mineral N(MN,NH4+-N plus NO3--N)was extracted with 2 mol?L-1KCl solution and measured by the indophenol blue method and the cadmium reduction method(Allen,1989).Available phosphorus(AP)was extracted with 0.5 mol?L-1NaHCO3and analyzed using the molybdenum-antimony colorimetric method.Total N(TN)and P(TP)were determined using the respective Kjeldahl and molybdenum-antimony colorimetric methods after the samples were digested with H2SO4.

2.4.Assessment of nutrient capture and translocation

Fine roots of woody tree species have been proved a heterogeneous system differing markedly in structure and function(Chen et al.,2015b).It has been well established that the distal lower-order roots(1–2 order roots)mainly serve in absorptive functions,while higher-order roots(3–5 order roots)mainly serve in transport functions(Kou et al.,2017).To assess the nutrient foraging potential of the roots,we calculated the root-soil accumulation factor(i.e.root nutrient capture,RSAF)in a relative manner as follows(Ye et al.,2014):

where NuARand NuSare the nutrient contents in absorptive roots and soils,respectively.

To investigate the translocation behaviors of nutrients from roots to twigs and leaves,the translocation factors(TFs)of individual nutrients among different tree tissues were calculated as the ratio of the nutrient concentrations in absorptive roots to transport roots,twigs and mature leaves.The TF values were calculated with Eqs.(2–4)(Wu et al.,2021):

where TFAR-TR,TFTR-TWand TFTR-MNdenote the respective TF values for nutrients from absorptive roots to transport roots and from transport roots to twigs and mature needles;NuAR,NuTR,NuTWand NuMNare the nutrient contents in absorptive roots,transport roots,twigs and mature needles,respectively.Larger TF values correspond to stronger nutrient translocation abilities.

2.5.Calculation of nutrient resorption efficiency

Nutrient resorption efficiency(RE)is the percentage reduction in the nutrient concentration between mature(NuMN)and senesced needles(NuSN)by accounting for the mass loss correction factor(MLCF)(Hayes et al.,2014):

where MLCF is a mass loss correction factor,which was calculated from the mass of mature and senesced needles or from the percentage of the needle mass lost during senescence.The MLCF value of conifers is 0.745(Vergutz et al.,2012).

2.6.Statistical analysis

Fig.2.Root nutrient capture of native and exotic pine trees in different plantation types.Data are expressed as means±standard error(n=5).Different lowercase letters indicate significant differences between pure and mixed plantations of native pine/exotic pine(p<0.05).The two-way ANOVA results are presented as an inset(ns p>0.05,＊p<0.05,＊＊p<0.01,and＊＊＊p<0.001).NRSAF,PRSAF:N and P accumulation from rhizosphere to absorptive roots(a,b).

Fig.3.Tree nutrient translocation from absorptive roots to transport roots,from transport roots to twigs,and from transport roots to mature needles of native and exotic pine trees in different plantation types.Data are expressed as means±standard error(n=5).Different lowercase letters indicate significant differences between pure and mixed plantations of native pine/exotic pine(p<0.05).The two-way ANOVA results are presented as an inset(ns p>0.05,＊p<0.05,＊＊p<0.01,and＊＊＊p<0.001).NAR-TR,PAR-TR:N and P translocation from absorptive to transport roots(a,b);NTR-TW,PTR-TW:N and P translocation from transport roots to twigs(c,d);NTR-MN,PTR-MN:N and P translocation from transport roots to mature needles(e,f).

Two-way analysis of variance(ANOVA)was used to examine the statistical significance of the mixture effect and species effect,as well as their interactions on the variables of soil chemical properties,nutrient contents in tree tissues and internal nutrient cycles of pine species.The differences among the four plantation types were analyzed by the oneway ANOVA and Duncan's multiple comparison tests,if the interaction between the mixture effect and species effect was significant(p<0.05).The relationship between the main variables of the tree internal nutrient cycles of pine species was tested by Pearson correlation.The standard p<0.05 level was used throughout as the threshold for statistical significance.All statistical analyses were performed using IBM SPSS(version 24.0,USA).

3.Results

3.1.Nutrient contents in rhizosphere soil and tree tissues

Fig.4.Needle nutrient resorption efficiencies of native and exotic pine trees in different plantation types.Data are expressed as means±standard error(n=5).Different lowercase letters indicate significant differences between pure and mixed plantations of native pine/exotic pine(p<0.05).The two-way ANOVA results are presented as an inset(ns p>0.05,＊p<0.05,＊＊p<0.01,and＊＊＊p<0.001).NRE,PRE:N and P resorption efficiencies(%)of needle(a,b).

The replanting of broadleaved trees significantly affected the contents of N and P in rhizosphere soil and tree tissues(Table 1).Specifically,soil mineral N and available P in mixed plantations were significantly higher than those in the two pure pine plantations,which were significantly affected by mixture effect,species effect,and their interactions(p<0.05).N and P in fine roots,including absorptive and transport roots,of the native pure pine plantation were higher than those of the mixed plantation,while exotic pine showed the opposite pattern.The N and P contents in the twigs and mature needles of the two pine species did not differ significantly between the pure and mixed plantations and were not affected by interactions between mixture and species effects.The replanting of broadleaved trees significantly reduced P in the senesced needles of native pine but had little effect on exotic pine.

3.2.Nutrient capture by absorptive roots

The capture of N and P was significantly influenced by mixture effect,species effect,and their interactions(p<0.05,Fig.2).N and P capture by native pine trees decreased by 57.92%and 38.89%,respectively,in the mixed plantation compared with pure plantation.The N and P capture of exotic pine did not differ between the pure and mixed plantations.

3.3.Nutrient translocation in trees

The effects of mixture and species effects on N and P translocation varied with elements and nutrient pools(Fig.3).Specifically,the replanting of broadleaved trees significantly increased N translocation from transport roots to twigs and mature needles of native pine by 40.74% and 27.98%,respectively(Fig.3c and e),and significantly increased P translocation from transport roots to twigs by 35.96%(Fig.3d).In contrast,P translocation from transport roots to twigs and mature needles of exotic pine decreased by 53.32%and 40.96%,but did not affect the root-to-shoot translocation of N(Fig.3).

Fig.5.Correlations between the main variables of internal nutrient cycles of native and exotic pine trees based on the Spearman correlation coefficient.The variable correlation matrix contrasts 22 variables listed down the autocorrelation line of native(a)and exotic(b)pine trees.Positive correlations are displayed in blue and negative correlations in red.The color intensity and the size of the circles are proportional to the correlation coefficients:strong correlations are indicated by large circles,whereas weak correlations are indicated by small circles.The colors of the scale bar denote the nature of the correlation,with 1 indicating a perfect positive correlation(dark blue)and-1 indicating a perfect negative correlation(dark red)between two traits.＊indicates a significant correlation at p<0.05;ns p>0.05,＊p<0.05,＊＊p<0.01,and＊＊＊p<0.001.(For interpretation of the references to color in this figure legend,the reader is referred to the Web version of this article.)

3.4.Nutrient resorption efficiency

Nitrogen resorption efficiency was significantly affected by mixture and species effects,while P resorption efficiency was only affected by the interaction of mixture and species effects(p<0.05,Fig.4).The replanting of broadleaved trees significantly increased the N and P resorption efficiencies of native pine by 4.87%and 13.33%,respectively.The N and P resorption efficiencies of exotic pine did not differ significantly between the pure and mixed plantations.

3.5.Correlations of the main variables of internal nutrient cycles

There were significant correlations between the nutrient pools of the two pine species(Fig.5).Specifically,the soil mineral N and available P of native pine were negatively correlated with absorptive root N and P,respectively,while exotic pine showed the opposite pattern(Fig.5a and b).NAR,NTR,NMNand NSNas well as PAR,PTR,PMNand PSNof native pine were positively correlated with each other(Fig.5a).NAR,NTRand NMNof exotic pine were negatively correlated with each other,while PAR,PTRand PMNwere positively correlated with each other(Fig.5b).In addition,the N capture of the two pine species was negatively correlated with NAR-TR,NTR-TWand NRE,and P showed a consistent pattern.

4.Discussion

4.1.Effect of mixed planting on nutrient contents in rhizosphere soil and trees

As expected,rhizosphere soil N and P around pine trees were higher in mixed plantations than in pure plantations(Table 1;Table S1).Generally,broadleaved tree litter with higher nutrient contents can increase soil N and P availability in mixed plantations by altering the amount and quality of below-and aboveground litter input(Wang et al.,2007;Eshel and Beeckman,2013)and release rate of nutrients during litter decomposition(Masuda et al.,2022).Furthermore,mixed planting enhanced microbial activity and biomass in rhizosphere soil of mixed pine plantations(Li et al.,2021),which accelerates litter decomposition and thus enhances soil nutrients(Zeugin et al.,2010;Li et al.,2022).These results are consistent with the hypothesis that the replanting of broadleaved trees improves soil N and P availability in coniferous plantations.

Our results showed that the shoot N and P contents of the two pine species did not increase with soil nutrient availability in mixed plantations(Table 1).Consequently,this result does not support our first hypothesis.The mechanism behind this result is most likely related to the N and P mobility within plants.Broadleaf trees generally have higher root biomass and faster growth rate than coniferous trees(Fin′er et al.,2007),and thus the belowground competition for nutrients in mixed plantations often alters the nutrient uptake capacity of conifers(Miller et al.,2007;Trinder et al.,2013;Simon et al.,2014),in turn affecting the allocation of N and P in trees.Notably,plants tend to maintain relatively high nutrient contents in their functionally active tissues(Mo et al.,2019).Trees transport nutrients from older senescent tissues to metabolically active ones to support new growth(Vergutz et al.,2012;Di et al.,2018).Therefore,the nutrients in mature tissues are insensitive to environmental changes,such as the needles of the two pine species in the mixed plantations.Bu et al.(2020)found that plantingS.superbain Chinese fir(Cunninghamia lanceolata)plantations did not affect the nutrients in young twigs and needles but significantly reduced those in older tissues.These results suggesting that a detailed study of nutrients in old tissues may be helpful to explore the internal nutrient cycles of trees.

4.2.Effects of interspecific interactions on root nutrient capture of the two pine species

Mixed planting reduced the N and P capture of native pine and decreased the fine root N and P contents(Table 1;Fig.2).Conversely,mixed planting increased the fine root N and P contents of exotic pine,although it had little effect on N and P capture(Table 1;Fig.2).Obviously,this result was consistent with previous studies reported that neighboring species can facilitate or inhibit nutrient uptake of target species(Fotelli et al.,2005;Cahill and McNickle,2011),which was in agreement with our second hypothesis.

Root traits and their variations can promote the diversity of nutrient acquisition strategies(Zemunik et al.,2015;Liu et al.,2021),which are induced by interspecific interactions.Root morphology that alters in response to interspecific competition,e.g.,higher fine root biomass and specific root length(SRL),are considered as strategies to promote nutrient acquisition and acclimate to nutrient competition(Yu et al.,2019;Bu et al.,2020).The functional roots of native pine trees exhibited lower biomass when grown withS.superbaroot than when it grown alone(Table S2).Possibly,interspecific competition reduced the absorptive roots biomass of native pine trees,thereby reducing their N and P capture ability(Fig.2).This indicated that interspecific interactions have a negative effect on root N and P capture of native pine trees.This finding was consistent with the neutral hypotheses that coevolution between native species often drives them to develop more extreme traits(Mouillot et al.,2013;Nagelkerke and Rossberg,2014),and interactions involving native plants could be detrimental(Coux et al.,2021).By contrast,the fine root biomass and SRL of exotic pine trees increased when grown withS.superbaas compared to being grown alone(Table S2).It has been previously observed that exotic species generally have more generalist traits,such as stress tolerance and niche divergence(Golivets and Wallin,2018),which allow them to interact with better neighboring species(García et al.,2014).This implies that high plasticity of root morphology may help exotic pine trees to adapt to the presence of neighboring species.Consequently,the interaction between exotic pine andS.superbahad a positive effect on root N and P capture of exotic pine trees.These results indicated that the root nutrient capture of plants in response to interspecific interactions were species-specific.

Moreover,plants would increase associations with mycorrhizal fungal partner to improve root foraging for soil nutrients(Cahill and McNickle,2011;Bergmann et al.,2020).Based on the study of Yan et al.(2019),the replanting of broadleaved trees decreased the mycorrhizal association rate of native pine trees,but increased that of exotic pine trees.Similarly,a study also reported that exotic pine trees exhibited higher mycorrhizal association rate than native pine trees after replantingS.superba(Liu et al.,2021).Thus,we speculate that mycorrhizal associations may be the key reason for N and P accumulation in functional roots of exotic pine trees.However,we caution that more experimentation is required that integrates root nutrient capture and mycorrhizal status.Our results showed that the belowground nutrient capture of the two pines largely depended on their interspecific interaction withS.superba.

4.3.Needle nutrient resorption of both pines in response to the replanting of broadleaved trees

Nutrient resorption mainly occurs during leaf senescence.Through this process,plants can maintain high nutrient levels in nutrient-poor environments,and this process plays a pivotal role in balancing the stoichiometric homeostasis of trees(Chen et al.,2021).A previous study showed that under high amounts of available N and P in soil,trees could afford to be less conservative with N and P in their leaves(Kou et al.,2017).However,neighboring species altered the resorption response to tree-level soil nutrients.Our results show that the replanting of broadleaved trees significantly increased the needle N and P resorption efficiencies of native pine but had no significant effect on exotic pine(Fig.4).These findings suggest that the aboveground nutrient resorption strategy was preferentially employed rather than the capture strategy for native pine to reduce N and P losses in the mixed plantations.Therefore,our third hypothesis was also supported.The mixed planting effects of N and P resorption differences between native and exotic pines depend in large part on the intensity of competition among the species.Accordingly,when examined more closely,decreased N and P resorption with increasing soil nutrient supply was found only in trees that competed fiercely.In highly competitive environments,the energetic cost generally increases in proportion to nutrient capture,as a vast amount of roots are needed for successful patch exploitation;thus,plants are more inclined to choose the resorption strategy(Hodge,2004;Huang et al.,2015).Therefore,these results show that nutrient resorption is not determined by soil nutrients alone but is more strongly regulated by interspecific interactions between pines and broadleaved trees.

Fig.6.Summary of the effects of mixed planting on the processes associated with the internal nutrient cycles of native and exotic pine trees and the corresponding nutrient capture-resorption trade-off of trees observed in this study.

4.4.The tree translocation of nutrient reflects the trade-off between root nutrient capture and needle nutrient resorption

We found that the NRSAFand NRE,as well as the PRSAFand PRE,of the two pines were negatively correlated with each other(Fig.5),indicating a trade-offs between N and P capture and resorption(Fig.6).The increase in N and P translocation from transport roots upward toward twigs and needles in native pine in mixed plantations reflects the priority of aboveground nutrient conservation(Fig.3).These results concur with previous findings that under nutrient stress,more N and P are transported to leaves for photosynthetic carbon assimilation to maintain tree growth(Mo et al.,2019).Conversely,the root-to-shoot translocation of N and P in exotic pine that decreased in the mixed plantation reflects the priority of belowground nutrient capture(Fig.3).Fine roots are the functional module associated with nutrient uptake and transport(McCormack et al.,2015),and more nutrients allocated to them may be beneficial to root growth and resource acquisition(Pregitzer et al.,2002).These results imply that exotic pine might become“smarter”in regulating N and P allocation in response to the replanting of broadleaved trees.

Despite these interpretations,caution should be exerted.First,there could be other controls on belowground nutrient capture and aboveground nutrient resorption,such as root production,turnover and phenology(Adams et al.,2013;McCormack et al.,2014),leaf lifespan(Eckstein et al.,1999),as well as climate(Reed et al.,2012)that were not considered in this study.Second,both N and P capture and translocation were estimated indirectly by calculating ratios of adjacent nutrient pools,rather than directly measured by tracers(32P and15N).These parameters only reflect the relative magnitude of nutrient concentrations between adjacent nutrient pools(Kou et al.,2017;Wu et al.,2021),uncertainties therefore,remain about the absolute sizes of the pools and their changes over time.

5.Conclusions

The replanting of broadleaved trees in originally pure plantations of both native and exotic pines increased N and P availability in rhizosphere soils but did not improve the nutrient contents in the pine trees in mixed plantations.Mixed planting had a negative effect on the nutrient capture of native pine,possibly due to the belowground nutrient competition between native pine andS.superba.In contrast,the interspecific interaction between exotic pine andS.superbahad a positive effect on nutrient capture of exotic pine,due to the more generalist traits of exotic pine.In mixed plantations,leaf nutrient resorption was preferentially used by native pine,whereas root nutrient capture was performed by exotic pine.The root-to-shoot translocation of N and P increased in native pines but decreased in exotic pines.Therefore,exotic pine may be more suitable than native pine for replanting withS.superba.

Our study highlights that the replanting of broadleaved trees altered the internal nutrient cycles of native and exotic pines in subtropical plantations.The responses of N and P capture,resorption and translocation to interspecific interactions between pine and broadleaved trees provide supplemental data for species selection to improve the structures of pure coniferous plantations in subtropical China.

Funding

This work was supported by the National Natural Science Foundation of China(Grant Nos.32171759,31730014).

Availability of data and materials

Available on request.

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

CRediT authorship contribution statement

Yong Lin:Conceptualization,Data curation,Formal analysis,Methodology,Writing–originaldraft,Writing–review&editing.Chengkang Xia:Validation,Visualization,Methodology,Software.Gaoyang Wu:Investigation,Data curation.Fangchao Wang:Project administration,Writing–original draft,Writing–review&editing.Shengnan Wang:Investigation,Data curation.Yuanqiu Liu:Data curation,Project administration,Supervision.Fusheng Chen:Conceptualization,Methodology,Funding acquisition,Project administration,Writing–original draft,Writing–review&editing.

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.

Acknowledgements

The authors would like to acknowledge the Jiangxi Provincial Key Laboratory of Silviculture,China for providing study space.In addition,all the authors are grateful to Prof.Xiaofei Hu and Xiangmin Fang for their support.

Appendix A.Supplementary data

Supplementary data to this article can be found online at https://doi.i.org/10.1016/j.fecs.2022.100067.

List of abbreviations

NP Native pine in pure plantation

NM Native pine in mixed plantation

EP Exotic pine in pure plantation

EM Exotic pine in mixed plantation

MNS,APSMineral nitrogen(N)and available phosphorus(P)contents in rhizosphere soil(mg?kg-1)

NAR,PARN and P contents in absorptive roots(mg?g-1)

NTR,PTRN and P contents in transport roots(mg?g-1)

NTW,PTWN and P contents in twigs(mg?g-1)

NMN,PMNN and P contents in mature needles(mg?g-1)

NSN,PSNN and P contents in senesced needles(mg?g-1)