Submitted 2 December 2019Accepted 11 September 2020Published 14 October 2020

Corresponding authorFenli Zheng flzhmsiswcaccn

Academic editorMark Tibbett

Additional Information andDeclarations can be found onpage 16

DOI 107717peerj10084

Copyright2020 Wang and Zheng

Distributed underCreative Commons CC-BY 40

OPEN ACCESS

Ecological stoichiometry of plant leaveslitter and soils in a secondary forest onChinarsquos Loess PlateauZongfei Wang12 and Fenli Zheng13

1 State Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau Institute of Soil and WaterConservation Chinese Academy of Sciences and Ministry of Water Resources Yangling China

2University of Chinese Academy of Sciences Beijing China3 Institute of Soil and Water Conservation Northwest AampF University Yangling China

ABSTRACTEcological stoichiometry can reveal nutrient cycles in soil and plant ecosystems andtheir interactions However the ecological stoichiometry characteristics of leaf-litter-soil system of dominant grasses shrubs and trees are still unclear as are their intrinsic re-lationship during vegetation restoration This study selected three dominant plant typesof grasses (Imperata cylindrica (I cylindrica) and Artemisiasacrorum (Asacrorum))shrubs (Sophora viciifolia (S viciifolia) and Hippophae rhamnoides (H rhamnoides))and trees (Quercus liaotungensis (Q liaotungensis) and Betula platyphylla (B platy-phylla)) in secondary forest areas of the Chinese Loess Plateau to investigate ecologicalstoichiometric characteristics and their intrinsic relationships in leaf-litter-soil systemsThe results indicated that N concentration and NP ratios in leaf and litter were highestin shrubland leaf P concentration in grassland was highest and litter in forestland hadthe highest P concentration Soil C N and P concentrations were highest in forestland(P lt 005) and declined with soil depth Based on the theory that leaf NP ratio indicatesnutritional limitation of plant growth this study concluded that grass and shrub growthwas limited by N and P element respectively and forest growth was limited by both ofN and P elements The relationships between the N concentration in soil leaf and litterwas not significant (P gt05) but the soil P concentration was significantly correlatedwith litter P concentration (P lt 005) These finding enhance understanding of nutrientlimitations in different plant communities during vegetation restoration and provideinsights for better management of vegetation restoration

Subjects Ecology Ecosystem Science Plant Science Soil ScienceKeywords Plant community type Leaf-litter-soil Ecological stoichiometry Nutrient elementsNutrient limitation

INTRODUCTIONSoil erosion remains a major global environmental problem accelerating soil nutrientlosses and ecosystem degradation (Luque et al 2013) Soil nutrient losses greatly decreasedsoil quality (Liu amp Dang 1993) which seriously threatens the stability of ecosystemsVegetation restoration is a powerful approach for ecological restoration of degradedlands as it can control soil erosion and improve ecosystem functions and services(Godefroid et al 2003 Zheng 2006 Jiao et al 2012 Sauer et al 2012 Zhao et al 2015

How to cite this article Wang Z Zheng F 2020 Ecological stoichiometry of plant leaves litter and soils in a secondary forest on ChinarsquosLoess Plateau PeerJ 8e10084 httpdoiorg107717peerj10084

Bienes et al 2016) Vegetation restoration areas currently cover approximately 020 billionha worldwide and are being planted at a rate of 45 million ha per year (Zhao et al 2015)Over time vegetation restoration can improve soil quality (Fu et al 2010) and accelerateN and P cycling in plants and soils (Luuml et al 2012) Vegetation restoration has resultedin species replacement which has changed the structure of the community and speciesdiversity (Wang et al 2011) and form a diverse ecosystem of trees shrubs and herbswhich results in changes in nutrients distribution in leaves litter and soil (Parfitt Yeates ampRoss 2005 Hobbie et al 2006 John et al 2007 Jiao et al 2013 Zhao et al 2017) Severalplant communities show significant differences in nutrient allocation due to different plantspecies throughout vegetation restoration (Warren amp Zou 2002 Schreeg et al 2014 Denget al 2016) Therefore it is necessary to quality nutrient characteristics in the leaf-litter-soilsystem of dominant grasses shrubs and trees as well as their intrinsic relationships duringvegetation restoration

Ecological stoichiometry describes the balance of energy andmultiple chemical elementsin ecosystems (Elser et al 2000) and has already become amethod for studying the stabilityand NP limitations of degraded ecosystems (Guumlsewell 2004 Han et al 2005) Ecologicalstoichiometry is also an effective tool to study the interactions between soils and plant andtheir nutrient cycles (Elser 2006) C N and P cycles account for the transfer of nutrientsbetween plant and soil C is a key building block of structural substances supplyingapproximately 50 of the dry biomass whereas N and P are the major limiting elementsof natural terrestrial ecosystems and both play important roles in several physiological andmetabolic processes These three nutrients elements interact with each other and both Nand P affect carbon fixation (Han et al 2005) The notion that leaf NP ratio can be usedto identify nutrient limitations for plant growth has been widely confirmed in variousplant communities (Koerselman amp Meuleman 1996 Schreeg et al 2014) The NP ratio ofplant leaves can be used to characterize the productivity of terrestrial ecosystems and itcan also indicate which elements of the plant are limited but this relationship can changewith changes in the environment (Guumlsewell 2004) Thus it provides a scientific basis forthe rational allocation of vegetation to investigate nutrient limitation of NP ratio in theprocess of vegetation restoration

In the plant-soil ecosystem litter serves as a main carrier of nutrients and links plantsand soil (Agren amp Bosatta 1998) The litter layer provides storage for ecosystems nutrientsand acts as a hub for material exchange between soils and plants and it is a naturalsource of soil fertility (Agren et al 2013) Nutrient supply in soil plant growth demandand litter return to soil are nominally independent factors but they also interact witheach other which leads to the complex relationship among nutrient concentrations inthe plant-litter-soil systems (Agren amp Bosatta 1998) Ecological stoichiometry provides aneffective approach for observing these relationship between nutrients in the plant-litter-soilsystems and their characteristics in ecological processes (Elser et al 2000) Thus it is oftheoretical and practical significance to analyze the ecological stoichiometric characteristicsof leaf-litter-soil systems during vegetation restoration

Due to its steep topography and erodible soil coupled with long-term human activitythe ecological environment of the Loess Plateau is extremely fragile and has become

Wang and Zheng (2020) PeerJ DOI 107717peerj10084 221

one of the most severely eroded areas of China (Jiao et al 2012 Zhao et al 2015) Inpast centuries the majority of forestlands were destroyed to satisfy the food needs of thegrowing population which resulted in severe soil erosion and land degradation The Grainto Green Program (GTGP)was implemented to control soil erosion and improve ecosystemdegradation with amain goal of converting low-yield steep-slope croplands into permanentvegetation cover (Jiao et al 2012 Zhao et al 2015) Vegetation restoration generated adiverse flora and reduced soil erosion raising interest in the characterization of thisrecovering ecosystem For example An amp Shangguan (2010) and Chai et al (2015) studiedleaf stoichiometric traits and concluded that the growth of vegetation was N-limited at eachsecondary successional stage according to the leaf NP threshold Ai et al (2017) observedthat the slope aspect had various effects on plant and soil CNP stoichiometry Variationsin vegetation types influenced soil CNP ratios which were higher in afforested lands thanin slope croplands (Zhao et al 2015 Deng et al 2016 Zhao et al 2017) Jiao et al (2013)studied soil stoichiometry during vegetation successional changes and reported that soilNP ratio increased with the vegetation restoration year It was even reported that forestage had a significant effect on C N P and K concentrations and their ratios in plant tissuesand soil (Li et al 2013) Most previous studies addressed the stoichiometric characteristicsof soil system and vegetation communities including forests and grasslands as well aslitter individually or in both However the ecological stoichiometry of the plant-litter-soilsystem as a whole has been rarely described (Zeng et al 2017 Cao amp Chen 2017) and theeffects of dominant plant communities (tree shrub grass) during vegetation restorationon this ecological stoichiometry remains poorly understood This will provide a betterunderstanding of nutrient limitation in different plant communities during vegetationrestoration and improve ecosystem management In addition the majority of previousstudies have focused on topsoil (Jiao et al 2013 Li et al 2013 Zeng et al 2016 Zeng et al2017) there is little information on stoichiometry change with the soil profile (Zhao et al2015 Deng et al 2016) Due to the depth of thick loess on the Loess Plateau the majorityplant roots are distributed within the top 100 cm Therefore it is important to investigatechange of the stoichiometry of C N and P with soil profile depth

Vegetation succession starts from annual grass then to perennial grass shrub forestafter farmlands are abandoned So three dominant plant communities of grasses (Imperatacylindrica and Artemisia sacrorum) shrubs (Sophora viciifolia and Hippophae rhamnoides)and trees (Quercus liaotungensis and Betula platyphylla) were selected in the Ziwulingsecondary area of the Loess Plateau to investigate ecological stoichiometry in the plant-litter-soil system and their intrinsic relationships The specific objectives of this study wereto (1) determine leaf and litter C N and P concentrations and their ecological stoichiometrycharacteristics in six dominant plant species (2) investigate distributions of soil C N andP concentrations and ecological stoichiometry characteristics in soil profile (3) examinethe relationships of ecological stoichiometry in leaf-litter-soil system (C N and P) and (4)assess the limiting nutrient element for plant growth in the six plant species The effort willprovide information about ecological stoichiometry and theoretical support for enhancingvegetation and ecosystem restoration on the Loess Plateau

Wang and Zheng (2020) PeerJ DOI 107717peerj10084 321

MATERIAL AND METHODSStudy site descriptionThis study site is located at Fuxian County Shanxi Province China (3554primeN 10989primeE)in the center of Loess Plateau south of the Yanrsquoan city The topography and landformbelong to loess hilly-gully region with elevation ranging from 920 to 1683 m (Zheng 2006)The mean annual temperature ranges from 6 to 10 C and mean annual precipitationsis between 600 to 700 mm The soil is mainly composed of loess which can be classifiedas a Calcic Cambisol (USDA NRCS 1999) The soil texture was 283 sand (gt50 microm)581 silt (50ndash2 microm) and 136 clay (lt2 microm) Vegetation of the Loess Plateau was almostcompletely removed more than 100 years ago and soil loss was 8000 to 10000 t kmminus2

yrminus1 (Zheng et al 1997 Kang et al 2014) In 1866ndash1870 the inner war happened in thisregion (Zhang amp Tang 1992 Tang et al 1993 Zheng et al 1997) and as population movedout and then secondary succession of vegetation began Currently forest canopy closureis more than 06 and dominant species for tree are Quercus liaotungensis (climax forestcommunity) and Betula platyphylla (early forest community) dominant species for shrubare Sophora viciifolia and Hippophae rhamnoides both does not concur in same placesand main grass species are Imperata cylindrica and Artemisia sacrorum (Zheng 2006) Thedistribution area of the above mentioned six dominant species occupies more than 70 oftotal area in the study site

Soil and plant samplingAccording to our field investigation there are 38 species in the study site including 18artificial species and 20 natural species which cover five tree species six shrub species ninegrass species Moreover the six tree shrub and grass species ie Quercus liaotungensisand Betula platyphylla (forest communities) Sophora viciifolia and Hippophae rhamnoides(shrub communities) and Imperata cylindrica and Artemisia sacrorum (grass communities)are dominant species and their distribution area occupies more than 70 of total areain the study site Other studies also reported that these six species are dominant speciesof natural vegetation succession (Zheng 2006 Wang Shao amp Shangguan 2010 Zhang ampShangguan 2016) Thus these six species have been selected to investigate to ecologicalstoichiometry of plant leaf litter and soil in a secondary forest on Chinarsquos Loess PlateauFor each dominant species three experimental sites (three replications) with a similarsite condition including slope position (slope length gradient and aspect) soil type andaltitude were set up to collect samples In addition the distance within all experimentalsites was within approximately 3 km which reduced impacts of previous site conditionPlant leaves and soil samples were collected in late July 2016 when plants were in a vigorousgrowth period and litter samples on the soil surface consisting of leaf fall over multipleyears that were not decomposed were obtained in late October 2016 Table 1 shows thecharacteristics of these three plant types

Two plots with 10 times 10 m size were established in each experimental site of forest typeand the plots sizes for shrub and grass types were 5 times 5 m and 1 times 1 m respectively Tento twenty complete expanded living and sun-exposed leaves were randomly collected fromfive to ten healthy individual plants per plot from shrubs or trees and a total of 80 to 100

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Table 1 Characteristics of the three plant types

Vegetationtypes

Dominant plantspecies

Abbreviation Accompanying plantspecies

Altitude(m)

Coverage () Slope degree()

Slopeaspect

Forest Quercus liaotungensisBetula platyphylla

Q liaotungensisB platyphylla

Carex lanceolata 13551133

6080

21ndash2517ndash20

WS260

WS120

Shrub Sophora viciifoliaHippophae rhamnoides

S viciifoliaH rhamnoides

Stipa bungeanaBuddleja alternifolia

12801332

5575

15ndash2015ndash17

WS255

WS45

Grass Imperata cylindricaArtemisia sacrorum

I cylindricaA sacrorum

Artemisia giraldiiThemeda japonica

13101336

7075

10ndash1215ndash20

WS259

WS220

leave samples were collected For each grass plot all stems and leaves were completely cutfrom three 025 m2 sampling areas Leaves from each plot were evenly mixed and then putinto a paper bag Litter samples were collected along the diagonal lines of three 1 times 1 msquares per plot and mixed and stored in paper bags All samples of leaves and litter werecarried back to the indoor laboratory for analysis

The total of 256 soil samples from a 100 cm-depth profile were collected using a 5-cmdiameter to collect soil samples along an S-shaped line in each plot Before each soil samplewas collected soil sampler was sterilized with ethanol to avoid cross-infection Moreoverthe 100 cm soil profile was divided into six layers (0ndash10 10ndash20 20ndash40 40ndash60 60ndash8080ndash100 cm) and soil samples from each layer were obtained from five points The fivesoil samples of each layer were mixed evenly and stored in plastic bags and then all soilsamples (6 plant speciestimes3 experimental sitestimes2 sample plotstimes6 soil sample layers) weretransported to the indoor laboratory

Sample analysisLeaf and litter samples were oven dried at 70 C for at least 48 h or more to reach a constantmass level and then weighed Dried plant samples were ground to a fine powder using aplant-samplemill (1093 SampleMill Foss Sweden) Soil samples were air-dried and sievedusing a 025 mmmesh To determine C concentration in plant and soil the Walkley-Blackmodified acid-dichromate FeSO4 titration method was used (Bao 2000) and the Kjeldahlmethod (KJELTE2300 Sweden) was applied to measure the total N concentration in plantand soil The total P concentration in plant was measured by using a SpectrophotometerUV-2300 (Techcomp Com Shanghai China) after digestion with H2SO4 and H2O2and the total P concentration in soil was determined by a spectrophotometer after wetdigestion with H2SO4 and HClO4 (Bao 2000) Leaf litter and soil C N P concentrationswere expressed as gkg on dry weight basis The CNP ratios in leaves litter and soil werecomputed as mass ratios

Statistical analysisAll data are presented as mean plusmn standard errors and tested for normality of distributionsand homogeneity of variances before analysis A one-way analysis of variance (ANOVA)wasused to analyze the effects of the plant type on nutrients and stoichiometric characteristicsin leaf litter and soil Two-way ANOVAs were computed to analyze the effects of plant typesoil depth and their interactions on soil C N and P concentrations and their stoichiometry

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Table 2 Nutrient concentrations and characteristics of ecological stoichiometry in leaves of the three plant types

Vegetationtypes

Plantspecies

C(gkg)

N(gkg)

P(gkg)

CN CP NP

Q liaotungensis 505plusmn 115Bb 187plusmn 098Ab 130plusmn 003Bc 271plusmn 086Ac 388plusmn 667Aa 143plusmn 055AcForest

B platyphylla 522plusmn 114Aa 181plusmn 100Ab 140plusmn 003Ab 290plusmn 204Ab 373plusmn 240Ab 129plusmn 015BdS viciifolia 499plusmn 962Ab 289plusmn 083Aa 128plusmn 003Bc 173plusmn 023Ad 390plusmn 108Aa 226plusmn 082Aa

ShrubH rhamnoides 502plusmn 122Ab 298plusmn 124Aa 142plusmn 003Ab 169plusmn 077Ad 354plusmn 123Bb 210plusmn 097BaI cylindrica 491plusmn 533Ab 104plusmn 032Bc 170plusmn 003Aa 473plusmn 173Aa 289plusmn 813Ac 612plusmn 021Bf

GrassA sacrorum 475plusmn 997Bc 179plusmn 038Ab 180plusmn 010Aa 266plusmn 078Bc 264plusmn 120Ac 993plusmn 071Ae

NotesBars indicate the standard errors (n= 6) The lowercase letters above the bars indicate significant differences in leaf at different plant types and the capital letters represent signif-icant differences in leaf at the same plant types of different species (P lt 005)

The linear regression analysis was used to test the relationship between C N and Pconcentrations in leaf litter and soil Pearson correlation was used to assess relationshipbetween leaf litter and soil stoichiometric characteristics Differences were consideredsignificant with a P lt 005 All statistical analyses were determined with SPSS 190 software(SPSS Inc Chicago IL USA)

RESULTSLeaf and litter nutrients and ecological stoichiometry in dominantplant communitiesThe leaf C N and P concentrations were different among plant communities (Table 2)The C concentration in leaf varied from 475 (grass) to 522 gkg (forest) and was highestin B platyphy lla and lowest in A sacrorum The leaf N concentration was 298 gkg inshrub and was significantly greater than in forest and grass (P lt 005) while the leaf Pconcentration with 180 gkg was highest in grass The leaf CN ratio varied from 169(shrub) to 473 (grass) and was highest in I cylindrica and lowest in H rhamnoides Theleaf CP ratio was significantly higher in Q liaotungensis and S viciifolia than other species(P lt 005) The leaf NP ratio varied from 612 (grass) to 226 (shrub) and was significantlyhigher in shrub than in grass and forest (P lt 005)

The C N and P concentrations in litter were significantly affected by plant types(Table 3) The litter C concentration varied from 360 (shrub) to 413 (forest) and wassignificantly higher in forest than in grass and shrub (P lt 005) N concentrations showeda similar pattern between litter and leaf and were significantly highest in shrub (P lt 005)The litter P concentration varied from 051 (grass) to 097 gkg (forest) and was highest inB platyphy lla and lowest in I cylindrica The litter CN and CP ratios in grass were 529and 735 respectively and were significantly higher than in forest and shrub (P lt 005) Thelitter NP ratio varied from 125 (forest) to 242 (shrub) and was highest in H rhamnoidesand lowest in B platyphy lla (P lt 005)

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Table 3 Nutrient concentrations and characteristics of ecological stoichiometry in litter of the three plant types

Vegetationtypes

PlantSpecies

C(gkg)

N(gkg)

P(gkg)

CN CP NP

Forest Q liaotungensis 398plusmn 115Aab 138 plusmn 082Ab 092plusmn 004Aa 291plusmn 253Bc 433plusmn 291Ad 149plusmn 038AcB platyphylla 413plusmn 154Aa 122plusmn 191Ac 097plusmn 010Aa 346plusmn 426Ab 431plusmn 353Ad 125plusmn 066Bd

Shrub S viciifolia 360plusmn 167Ac 175plusmn 112Aa 075plusmn 006Ab 207plusmn 148Ad 486plusmn 510Ac 235plusmn 152AaH rhamnoides 360plusmn 262Ac 177plusmn 056Aa 074plusmn 006Ab 204plusmn 200Ad 489plusmn 292Abc 242plusmn 227Aa

Grass I cylindrica 375plusmn 126Abc 712plusmn 048Bd 051plusmn 003Bc 529plusmn 384Aa 735plusmn 427Aa 140plusmn 161BcA sacrorum 395plusmn 174Aab 120plusmn 069Ac 073plusmn 004Ab 330plusmn 243Bb 543plusmn 422Bb 165plusmn 053Ab

NotesBars indicate the standard errors (n= 6) The lowercase letters above the bars indicate significant differences in litter at different plant types and the capital letters represent sig-nificant differences in litter at the same plant types of different species (P lt 005)

Soil nutrients and ecological stoichiometry in dominant plantcommunities and soil depthsPlant type and soil depth had significant effects on soil nutrients and their CNP ratios(Table 4) Soil C and N concentrations in forestland were greater than in shrublandand grassland at all soil depths and both were highest in Q liaotungensis and lowest inA sacrorum (P lt 005) Soil P concentration in shrubland was lower than in grassland andforestland at every soil depth (P lt 005) and there were no differences in B platyphyllaQ liaotungensis and A sacrorum at 20ndash100 cm soil depths Soil CN ratio in forestlandwas significantly higher than in shrubland and grassland at both 0-10 and 10ndash20 cm soildepths (P lt 005) but there were no significant differences at 20ndash100 cm soil depths(P gt 005) Soil CP and NP ratios in forestland was significantly higher than in shrublandand grassland at both 0-10 and 10ndash20 cm soil depths (P lt 005) but both were highest inshrubland at 20ndash100 cm soil depths (P lt 005)

Soil depth is a driving factor for soil nutrient concentrations and their ratios (Table 4and Fig 1) Soil C and N concentrations significantly decreased with soil sampling depthSoil C and N concentrations decreased markedly from 10 to 40 cm of soil depth and thenslightly decreased from 40 to 100 cm Soil P concentration tended to stable with the soilsampling depth Soil CN ratio fluctuated with depth and soil CP and NP ratios had thesame trend along the soil sampling depth and decreased markedly from 10 to 40 cm of soildepth and then slightly decreased from 40 to 100 cm

The results of the Two-way ANOVA analysis indicated that both plant type and soildepth significantly affected the soil C N and P concentrations and their stoichiometry(CN CP and NP ratios) The interactions between plant type and soil depth significantlyaffected the soil C and N concentrations and CN CP and NP ratios but not soil Pconcentration (Table 5)

Relationships between C N and P concentrations and theircharacteristics of ecological stoichiometry among leaf litter and soilThere were significant correlations between leaf and litter for both N and P concentrationsin three plant community types (P lt 005) (Figs 2B 2C) The relationships between theplant C concentration and soil C concentration were significant in two soil layers (0ndash10

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Table 4 Profile distribution of soil nutrient concentrations and characteristics of ecological stoichiometry at different community types

Vegetationcommunity

Soillayer (cm)

C(gkg) N(gkg) P(gkg) CN CP NP

0ndash10 219plusmn 069Aa 183plusmn 013Aa 070plusmn 002Ab 120plusmn 053Aa 315plusmn 149Aa 264plusmn 022Aa

10ndash20 126plusmn 059Ba 099plusmn 002Ba 066plusmn 003Bab 127plusmn 056Aa 191plusmn 148Ba 150plusmn 006Bb

20ndash40 551plusmn 041Ca 061plusmn 006Ca 064plusmn 002BCa 913plusmn 06Ca 865plusmn 069Cb 091plusmn 009Cb

40ndash60 425plusmn 024Dab 049plusmn 004Da 062plusmn 002Cb 872plusmn 032Cc 688plusmn 027Dcd 079plusmn 006Dab

60ndash80 404plusmn 025 Dab 043plusmn 003Da 063plusmn 002Ca 949plusmn 029BCa 640plusmn 032Dbc 067plusmn 003DEbc

Q liaotungensis

80ndash100 394plusmn 025 Da 040plusmn 006Da 063plusmn 002Ca 955plusmn 091Ba 628plusmn 018Dbc 064plusmn 007Ebc

0ndash10 190plusmn 165Ab 167plusmn 070Ab 074plusmn 005Aa 113plusmn 057Aab 257plusmn 104Ab 227plusmn 007Ab

10ndash20 113plusmn 065Bb 097plusmn 006Ba 069plusmn 003ABa 117plusmn 031Ab 162plusmn 042Bb 139plusmn 005Bc

20ndash40 546plusmn 041Ca 059plusmn 004Ca 066plusmn 003BCa 928plusmn 128Ca 832plusmn 064Cb 091plusmn 007Cb

40ndash60 448plusmn 053CDa 047plusmn 005Dab 065plusmn 003BCa 945plusmn 057Cabc 695plusmn 095Dabc 074plusmn 009Dc

60ndash80 422plusmn 022Da 040plusmn 003Eab 064plusmn 006BCa 106plusmn 103ABa 671plusmn 102Dbc 063plusmn 007Ebc

B platyphylla

80ndash100 369plusmn 032Dab 037plusmn 003Eab 062plusmn 005Ca 993plusmn 094BCa 598plusmn 076Dbc 061plusmn 008Ec

0ndash10 154plusmn 094Ac 143plusmn 009Ac 060plusmn 003Ac 108plusmn 117Ab 258plusmn 132Ab 241plusmn 019Ab

10ndash20 958plusmn 069Bc 089plusmn 002Bb 058plusmn 001Ac 108plusmn 092ABc 167plusmn 096Bb 155plusmn 005Bb

20ndash40 527plusmn 041Cab 057plusmn 003Ca 058plusmn 003Ab 926plusmn 035Ca 913plusmn 039Cb 099plusmn 004Cb

40ndash60 398plusmn 038Dc 043plusmn 008Dabc 054plusmn 000Bc 948plusmn 116BCabc 738plusmn 070Dbc 080plusmn 015Dab

60ndash80 352plusmn 029Dc 037plusmn 006Deb 052plusmn 000Bb 979plusmn 108ABCa 676plusmn 038Dbc 070plusmn 011Db

S viciifolia

80ndash100 340plusmn 020Dc 033plusmn 003Ec 052plusmn 001Bb 103plusmn 051ABCa 655plusmn 049Db 064plusmn 005Dbc

0ndash10 119plusmn 112Ad 111plusmn 008Ae 049plusmn 001Ad 108plusmn 081Ab 241plusmn 207Ab 225plusmn 014Ab

10ndash20 811plusmn 056Bd 085plusmn 005Bb 045plusmn 003Bd 955plusmn 082ABd 181plusmn 194Ba 190plusmn 016Ba

20ndash40 445plusmn 019Cc 048plusmn 001Cb 042plusmn 0001Cc 931plusmn 039Ba 107plusmn 067Ca 115plusmn 005Ca

40ndash60 380plusmn 027CDc 038plusmn 003Dc 042plusmn 001Cd 101plusmn 108abAB 908plusmn 066CDa 091plusmn 008Da

60ndash80 361plusmn 008Dc 035plusmn 003Db 042plusmn 001Cc 103plusmn 106ABa 861plusmn 064Da 084plusmn 008Da

H rhamnoides

80ndash100 340plusmn 022Dc 036plusmn 004Dab 043plusmn 002Cc 956plusmn 104ABa 801plusmn 029Da 085plusmn 009Da

0ndash10 132plusmn 105Ad 127plusmn 006Ad 064plusmn 002Ac 104plusmn 043Abc 207plusmn 101Ac 199plusmn 003Ac

10ndash20 893plusmn 072Bc 086plusmn 007Bb 060plusmn 003Bc 105plusmn 026Ac 148plusmn 047Bc 142plusmn 005Bc

20ndash40 503plusmn 053Cab 058plusmn 001Ca 058plusmn 002Bb 872plusmn 090Bab 869plusmn 102Cb 100plusmn 005Cb

40ndash60 420plusmn 027CDab 041plusmn 006Db 054plusmn 001Cc 105plusmn 123Aa 774plusmn 056CDb 075plusmn 010Dc

60ndash80 370plusmn 037Dbc 037plusmn 003Dbc 052plusmn 002CDb 101plusmn 101Aa 709plusmn 061Db 071plusmn 007Db

I cylindrica

80ndash100 368plusmn 042Dab 036plusmn 005Dab 050plusmn 001Db 104plusmn 141Aa 734plusmn 076Da 072plusmn 010Db

0ndash10 896plusmn 029Ae 092plusmn 002Af 068plusmn 003Ab 974plusmn 038ABc 132plusmn 067Ad 136plusmn 011Ad

10ndash20 731plusmn 028Bd 078plusmn 005Bc 065plusmn 003Bb 946plusmn 040Bd 112plusmn 034Bd 119plusmn 005Bd

20ndash40 474plusmn 037Cbc 059plusmn 006Ca 064plusmn 002BCa 802plusmn 031Cb 745plusmn 043Cc 093plusmn 007Cb

40ndash60 406plusmn 019Dab 045plusmn 004Dabc 062plusmn 001CDab 917plusmn 048Bbc 652plusmn 019Dd 071plusmn 006Dc

60ndash80 360plusmn 036Ec 037plusmn 002Eb 061plusmn 002CDa 988plusmn 132ABa 590plusmn 046Ec 060plusmn 04Ec

A sacrorum

80ndash100 349plusmn 027Ec 034plusmn 003Ec 061plusmn 0 02Da 104plusmn 054Aa 576plusmn 033Ec 055plusmn 003Ec

NotesBars indicates the standard errors (n= 6) The lowercase letters above the bars indicate significant differences in different plant species at the same four soil layers and the capitalletters represent significant differences in different soil layers at the same plant species (P lt 005)

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Figure 1 Concentrations of soil C N P and their ecological stoichiometry in the different samplingsoil layers of the different plant species (A) Soil C concentration in the different sampling soil layers ofthe different plant species (B) Soil N concentration in the different sampling soil layers of the differentplant species (C) Soil P concentration in the different sampling soil layers of the different plant species(D) Soil CN ratio in the different sampling soil layers of the different plant species (E) Soil CP ratio inthe different sampling soil layers of the different plant species (F) Soil NP ratio in the different samplingsoil layers of the different plant species Bars indicates the standard errors (n= 6) The lowercase lettersabove the bars indicate significant differences in different plant species at the same soil layers and the cap-ital letters represent significant differences in different soil layers at the same plant species (P lt 005) Icand As represent I cylindrica and A sacrorum respectively Hr and Sv represent H rhamnoides and S vici-ifolia respectively Bp and Ql represent B platyphylla and Q liaotungensis respectively

Full-size DOI 107717peerj10084fig-1

Wang and Zheng (2020) PeerJ DOI 107717peerj10084 921

Table 5 Correlations among ecological stoichiometry in leaf litter and soil at 0ndash10 0ndash20 and 0ndash100 cm soil depth

Factor F (P)valueC N P CN CP NP

Plant type 153(lt00001b)

814(lt00001)

315(lt00001)

490(00003)

125(lt00001)

721(lt00001)

Soil depth 1999(lt00001)

1701(lt00001)

516(lt00001)

224(lt00001)

1859(lt00001)

1226(lt00001)

Plant typeSoil deptha

541(lt00001)

304(lt00001)

035(00663)

354(lt00001)

401(lt00001)

188(lt00001)

NotesaIndicates the interaction between plant type and soil depthbparentheses is P value

and 0ndash20) and the profile (0ndash100 cm) (P lt 005) (Figs 3A 3B 3C and Figs 4A 4B4C) while there were no significant correlation between plant N concentration and soilN concentration (Figs 3D 3E 3F and Figs 4D 4E 4F) In the three plant communitytypes there were no significant correlations between leaf P concentration and soil Pconcentration (Figs 3G 3H 3I) but the soil P concentration was significant correlatedwith litter P concentration in 0ndash10 cm soil depth (P lt 005) (Fig 3G)

For the three plant community types leaf CN and NP ratios were positively correlatedwith litter CN and NP ratios respectively (P lt 005) (Figs 2D 2F) while leaf CP ratiowas negatively correlated with litter CP ratio (P lt 005) (Fig 2E) Leaf CP had a positivecorrelation with soil CP ratio at the 0ndash10 cm soil layer and over 0ndash100 cm soil profile(P lt 005) (Table 6) Leaf NP ratio had a positive correlation with soil NP ratio at twosoil layers (0ndash10 and 0ndash20 cm) and the profile (0ndash100 cm)(P lt 005) (Table 6) and therewas significant correlation between leaf and soil CN ratio at the 0ndash10 and 0ndash20 cm soillayers (P lt 005) (Table 6) At the 0ndash10 cm soil layer there was a significant correlationbetween litter and soil CN ratio (P lt 005) (Table 6) and litter CP ratios were negativelycorrelated with CP ratios at two soil layers (0ndash10 and 0ndash20 cm) and the profile (0ndash100cm) and only in the profile (0ndash100 cm) did litter NP ratio have a positive correlation withsoil NP ratio (P lt005) (Table 6)

DISCUSSIONImpacts of dominant plant communities on leaf and litter nutrientsand ecological stoichiometryAs a key subsystem plants have a vital function in governing the stability of terrestrialecosystem C N and P are essential nutrients for plant (Han et al 2005 John et al2007) and their interaction regulate plant growth (Guumlsewell 2004) Litter is one mainway for nutrients to return to the soil and is an important part of the forest ecosystemThe decomposition of plant litter replenishes soil nutrients to provide conditions forthe adjustment and demand of the plant nutrients (Agren amp Bosatta 1998) There aredifferences in the types quantity and utilization efficiency of absorbed nutrients in differentplants types In this study the results indicated that leaf C N and P concentrations differedacross plant communities The reason is that different plant communities has different

Wang and Zheng (2020) PeerJ DOI 107717peerj10084 1021

Figure 2 Relationships between leaf and litter C N P stoichiometric characteristics (A) The relation-ships between leaf and litter C concentrations (B) The relationships between leaf and litter N concentra-tions (C) The relationships between leaf and litter P concentrations (D) The relationships between leafand litter CN ratios (E) The relationships between leaf and litter CP ratios (F) The relationships be-tween leaf and litter NP ratios

Full-size DOI 107717peerj10084fig-2

adaptability to the environment and possess different strategies of nutrient adaptation(Wright et al 2004 Han et al 2005 Zheng amp Shangguan 2007 He et al 2008 Wu et al2012) In this study leaf C concentration in forest species was significantly higher thanin grass and shrub species while the leaf P in forest species was significantly lower thanin grass species An explanation may be that trees construct nutrient poor woody tissues

Wang and Zheng (2020) PeerJ DOI 107717peerj10084 1121

Figure 3 Relationships between leaf and soil C N and P concentrations in 0ndash100ndash20 cm soil depthsand 0ndash100 cm soil profile (A) The relationships between leaf and soil C concentrations in 0ndash10 soil depth(B) The relationships between leaf and soil C concentrations in 0ndash20 soil depth (D) The relationships be-tween leaf and soil C concentrations in 0ndash100 cm soil profile (D) The relationships between leaf and soilN concentrations in 0ndash10 soil depth (E) The relationships between leaf and soil N concentrations in 0ndash20soil depth (F) The relationships between leaf and soil N concentrations in 0ndash100 cm soil profile (G) Therelationships between leaf and soil P concentrations in 0ndash10 soil depth (H) The relationships between leafand soil P concentrations in 0ndash20 soil depth (I) The relationships between leaf and soil P concentrationsin 0ndash100 cm soil profile

Full-size DOI 107717peerj10084fig-3

while grasses do not The results are consistent with those of Wright et al (2004) whichreported that the leaf P concentration in herbaceous plants is significantly higher than inwoody plants Moreover in this study the C N and P concentrations in plant leaves werehigher than in the corresponding litter which was consistent with previous studies (Panet al 2011 Zeng et al 2017) Pan et al (2011) showed that the C N and P concentrationsin the leaves of trees shrubs and grasses were significantly higher than in litter likely dueto the reabsorption processes Previous studies have shown that nutrients present in leavesare transferred to flowers fruits branches and roots before leaf falling thereby preventingnutrients loss (Schreeg et al 2014) The results showed that N and P concentrations inlitter varied greatly in different plant communities and were significantly higher in treesthan in grasses This is because tree and shrub are deep-rooted plants and have the strong

Wang and Zheng (2020) PeerJ DOI 107717peerj10084 1221

Figure 4 Relationships between litter and soil C N and P concentrations in 0ndash100ndash20 cm soil depthsand 0ndash100 cm soil profile (A) The relationships between litter and soil C concentrations in 0ndash10 soildepth (D) The relationships between litter and soil C concentrations in 0ndash20 soil depth (C) The relation-ships between litter and soil C concentrations in 0ndash100 cm soil profile (D) The relationships between lit-ter and soil N concentrations in 0ndash10 soil depth (E) The relationships between litter and soil N concen-trations in 0ndash20 soil depth (F) The relationships between litter and soil N concentrations in 0ndash100 cm soilprofile (G) The relationships between litter and soil P concentrations in 0ndash10 soil depth (H) The rela-tionships between litter and soil P concentrations in 0ndash20 soil depth (I) The relationships between litterand soil P concentrations in 0ndash100 cm soil profile

Full-size DOI 107717peerj10084fig-4

capability of absorbing nutrients from multiple sources in the environment while grasseshave shallow roots and rely more on the recycling of their own nutrients

N and P elements are major limiting factors for plant growth in terrestrial ecosystemsand the leaf NP ratio could be used as an indicator to identify the limiting nutrient factors(Koerselman amp Meuleman 1996 Guumlsewell 2004) However the threshold of NP ratio isaffected by study area plant growth stage and plant species (Guumlsewell 2004) Guumlsewell(2004) reported that leaf NP ratio can be used to reveal N-limitation (NP ratio lt 10)or P-limitation (NP ratio gt 20) in the ecosystem In this study based on the Guumlsewellrsquosproposal that leaf NP ratio indicates nutritional limitation for plant growth we concludedthat grass and shrub growth was limited by N and P element respectively whereas forestgrowth was co-limited by both of N and P elements together in the research area In thisstudy the leaf NP ratio in S viciifolia and H rhamnoides were 226 and 210 respectively

Wang and Zheng (2020) PeerJ DOI 107717peerj10084 1321

Table 6 Correlations among ecological stoichiometry in leaf litter and soil in 0ndash100ndash20 cm soil depths and 0ndash100 cm soil profile

Nutrientratio

Soil depth (cm)

0ndash10 0ndash20 0ndash100

Soil CN Soil CP Soil NP Soil CN Soil CP Soil NP Soil CN Soil CP Soil NP

Leaf CN minus0344 minus0667 minus0737 minus0254 minus0732 minus0880 minus0381 minus0880 minus0813

Leaf CP 0508 0693 0646 0672 0640 0466 0135 0133 minus0016Leaf NP 0329 0643 0706 0261 0678 0792 0214 0676 0632

Litter CN minus0395 minus0708 minus0758 minus0303 minus0762 minus0886 minus0305 minus0874 minus0809

Litter CP minus0661 minus0839 minus0786 minus0670 minus0839 minus0759 minus0562 minus0712 minus0502

Litter NP minus0092 0183 0313 minus0273 0258 0542 minus0108 0591 0721

NotesCorrelation is significant at the 005 level (2-tailed)Correlation is significant at the 001 level (2-tailed)

suggesting that shrub growth was P-limited The leaf NP ratios in Q liaotungensis and Bplatyphylla were 143 and 129 respectively indicating that their growths were co-limitedby both N and P The leaf NP ratios in A sacrorum and I cylindrica were 612 and993 respectively indicating that grass growth was limited by N The results indicated thatdifferent plant communicates had different nutrient limiting elements which was consistedwith previous studies (Han et al 2005) The reason is that grass species (I cylindrica andA sacrorum) is a shallow-rooted plant with a strong ability to absorb soil surface nutrientsparticularly it has a greater capacity of relocating its leaf P before leaf falling than forestand shrub species and it can more effectively utilize leaf P concentration to meet growthdemands Moreover the biochemistry of the grass organic structure determines that morenitrogen is needed for growth Therefore grass species were less limited by P elementthan by N element In addition the results indicated that the growth of shrub species waslimited by P element which was similar to results reported by Han et al (2005) This isbecause S viciifolia and H rhamnoides are inherent species in vegetation restoration onthe Loess Plateau and were nitrogen-fixing plants and the absorption on of N elementis far greater than that of P element which results the shrub species to be limited by Pelement Furthermore the result showed that leaf CN and CP ratios were lower than inlitter which is consistent with results reported by McGroddy Daufresne amp Heedin (2004)indicating that the reabsorption capacity for C is lower than for N and P Although leaf NPratio can effectively reflect N or P limitation the importance of the NP ratio is mainly inits function as an indicator (Guumlsewell 2004) If the leaf NP ratio is to be used as an indexto evaluate both N and P nutrient supplies in the Loess Plateau further diagnosis regardingnutrient limitations should be conducted

Impacts of dominant plant communities on soil nutrient andecological stoichiometryPlants play an important role in improving soil fertility and contribute to the accumulationof soil nutrients Fu et al (2010) found that vegetation restoration could improve the netfixation of C and N and reduce their losses However the performance in soil quality

Wang and Zheng (2020) PeerJ DOI 107717peerj10084 1421

recovery differed among plant communities (Jiao et al 2012 Zeng et al 2016 Deng et al2016 Zhao et al 2017) In this study soil C N and P concentrations in forestland wasgreater than in grassland and shrubland which is consistent with the previous results of Jiaoet al (2012) andQi et al (2015) This result could be explained by a larger amounts of litterpresent in forestland a more above-ground litter and a higher volume of root exudatesreaching the soil resulting in higher nutrient concentrations in the forestland than in otherplant communities Soil C and N concentrations decreased with increasing of soil depthwhile soil P concentrations were relatively stable with depth which was consistent withWei et al (2009) The reasons might be the influence of soil parent material the amountnutrient content of returning litter the rate of decomposition and plant nitrogen fixationabsorption and utilization With an increasing of soil depth the input of organic mattergradually decreased (Nelson Schoenau amp Malhi 2008) However soil P is mainly derivedfrom rock weathering and leaching and its mobility is very low which caused verticalvariation of P along the soil profile to be relatively stable (Wei et al 2009)

Soil CNP ratios are important indicators of organicmatter composition soil quality andnutrient supply capacity (Bui amp Henderson 2013) In this study soil CNP ratios amongthe three plant communities were 169171 250231 and 286251 at the topsoil (0ndash10cm) respectively (Table 2) These values are substantially lower than the average globalvalue of 186131 (Clevel amp Liptzin 2007) Loess soils are naturally low in C meanwhilethe Loess Plateau has undergone a serious soil erosion prior to recent efforts at vegetationrestoration resulting in a low CNP ratio In this study soil CN ratio across differentplant communities and soil depths was approximately 108 in the Loess Plateau which wassimilar to the average level (119) in China (Tian et al 2010) but lower than the worldrsquosaverage value of 133 (Clevel amp Liptzin 2007) Previous studies showed that soil CN ratio isnegatively correlated with the decomposition rate of organic matter and low soil CN ratioindicates that organic matter is well decomposed (Zhao et al 2015 Deng et al 2016) Thesoil CN ratio in grassland shrubland and forestland was 101 108 and 117 respectivelyimplying that organic matter had been completely decomposed The soil CN ratio ineach plant community maintained relative stability with increasing soil depth which isconsistent with previous studies (Tian et al 2010) This may be due to the same changedynamics in C and N Soil CP and NP ratios in each plant community decreased withincreasing soil depth which may be due to the difference in the source of soil C N and PFurthermore this study showed that soil CP and NP ratios in forestland was higher thanin shrubland and grassland in the topsoil depth which may be due to the fact that foresthad more above-ground biomass than shrubland and grassland (Qi et al 2015)

Relationships between C N and P concentrations and theircharacteristics of ecological stoichiometry among leaf litter and soilSome previous studies have showed a strong correlation between leaf and soil nutrients(Parfitt Yeates amp Ross 2005 Agren amp Bosatta 1998 Agren 2008) while others found thatthere was no correlation between N and P concentrations in leaf and soil (Ladanai Agrenamp Olsson 2010 Yu et al 2010) In this study no significant correlation was found betweensoil N concentration with leaf N concentration for three plant community types One

Wang and Zheng (2020) PeerJ DOI 107717peerj10084 1521

possible reason is that through long-term adaptation to the habitat the N concentrationin plant leaves in this region may be more affected by the attributes of the species than thelimitation of soil nutrients In addition Reich amp Oleksyn (2004) showed that the mineralelements of plants are a combination of climate soil nutrients and species compositionOther studies have suggested that soil temperature soil water concentration microbialactivity and other factors have a greater impact on the mineral elements of plants (Chapinamp Pastor 1995 Guumlsewell 2004) In this study there was a significant correlation betweenlitter N and P concentrations and their ratios with leaf N and P concentrations amongthe three plant types indicating that the nutrients in litter were derived from plant leavesIn addition a strong correlation between soil and litter for both C and P concentrationsamong the three plant types was observed As a considerable portion of C and othernutrients elements in the litter could be released into the soil such that litter was one ofthe main sources of soil nutrients (Agren et al 2013) In general this study showed thatthere is a close correlation between the concentrations of C N and P and their ratios inleaf litter and soil in three plant community types which confirmed that C N and P inthe ecosystem were transported and transformed among plants litter and soil (McGroddyDaufresne amp Heedin 2004)

CONCLUSIONThis study analyzed C N and P concentrations and their stoichiometric characteristics inleaf litter and soil of three dominant plant types grass (I cylindrica and A sacrorum))shrubs (S viciifolia and H rhamnoides) and tree (Q liaotungensis and B platyphylla))during vegetation restoration on the Loess Plateau of China The results indicated thatplant community type had significant effects on leaf litter and soil nutrient concentrationsand their stoichiometry characteristics Grass species had highest leaf P concentrationand forest species litter had highest P concentration Leaf C N and P concentrationswere higher than in litter and soil (P lt 005) and forest community type had highest soilnutrient concentrations at all soil layers and their ecological stoichiometries were highestin topsoil (P lt 005) In addition soil CNP ratios in all plant communities decreasedwith increasing soil depth Soil P concentration and NP ratio had significant positivecorrelations with litter P concentration and NP ratio for the three plant community types(P lt 005) respectively However there were no significant correlations between soil NP concentrations and NP ratio with leaf N and P concentrations and NP ratio (P gt 05)respectively Based on the theory that leaf NP ratio indicates nutritional limitation forplant growth this study concluded that plant growth of the forest community type (Qliaotungensis and B platyphylla species) was co-limited by both of N and P elements plantgrowth of shrub community type (H rhamnoides and S viciifolia species) was limited by Pelement and grass growth (I cylindrica and A sacrorum species) was limited by N elementThese results can provide a scientific basis for the reconstruction of degraded ecosystemon the Loess Plateau of China

Wang and Zheng (2020) PeerJ DOI 107717peerj10084 1621

ACKNOWLEDGEMENTSThe authors are indebted to the anonymous reviewers and editors for their thoughtfulcomments and valuable suggestions and the authors also thank Dr Glenn V Wilson forcorrecting the English

ADDITIONAL INFORMATION AND DECLARATIONS

FundingThis study was financially supported by the External Cooperation Program of ChineseAcademy of Sciences (Grant No 161461KYSB20170013) The funders had no role in studydesign data collection and analysis decision to publish or preparation of the manuscript

Grant DisclosuresThe following grant information was disclosed by the authorsExternal Cooperation Program of Chinese Academy of Sciences 161461KYSB20170013

Competing InterestsThe authors declare there are no competing interests

Author Contributionsbull Zongfei Wang conceived and designed the experiments performed the experimentsanalyzed the data prepared figures andor tables authored or reviewed drafts of thepaper and approved the final draftbull Fenli Zheng conceived and designed the experiments performed the experimentsauthored or reviewed drafts of the paper and approved the final draft

Data AvailabilityThe following information was supplied regarding data availability

The raw measurements are available in File S1

Supplemental InformationSupplemental information for this article can be found online at httpdxdoiorg107717peerj10084supplemental-information

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Wang and Zheng (2020) PeerJ DOI 107717peerj10084 1721

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Cao Y Chen YM 2017 Coupling of plant and soil CNP stoichiometry in blacklocust (Robinia pseudoacacia) plantations on the Loess Plateau China Trees31(5)1559ndash1570 DOI 101007s00468-017-1569-8

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Clevel CC Liptzin D 2007 CNP stoichiometry in soil is there a lsquolsquoRedfield ratiorsquorsquo for themicrobial biomass Biogeochemistry 85(3)235ndash252 DOI 101007s10533-007-9132-0

Deng J Sun PS Zhao FZ Han XH Yang GH Feng YZ Ren GX 2016 Soil C N P andits stratification ratio affected by artificial vegetation in subsoil Loess Plateau ChinaPLOS ONE 11(3)e0151446 DOI 101371journalpone0151446

Elser J 2006 Biological stoichiometry a chemical bridge between ecosystem ecol-ogy and evolutionary biology The American Naturalist 168(S6)S25ndashS35DOI 101086509048

Elser JJ Sterner RW Gorokhova E FaganWF Markow TA Cotner JB Harrison JFHobbie SE Odell GMWeider LJ 2000 Biological stoichiometry from genes toecosystems Ecology Letters 3(6)540ndash550 DOI 101007s100210000027

Fu XL ShaoMAWei XR Horton R 2010 Soil organic carbon and total nitrogenas affected by vegetation types in Northern Loess Plateau of China Geoderma155(1)31ndash35 DOI 101016jgeoderma200911020

Godefroid S MassantWWeyembergh G KoedamN 2003 Impact of fencing onthe recovery of the ground flora on heavily eroded slopes of a deciduous forestEnvironmental Resource Management 32(1)62ndash76 DOI 101007s00267-002-2705-8

Guumlsewell S 2004 NP ratios in terrestrial plants variation and functional significanceNew Phytologist 164(2)243ndash266 DOI 101111j1469-8137200401192x

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He JS Wang L Dan FBFWang XP MaWH Fang JY 2008 Leaf nitrogen phospho-rus stoichiometry across Chinese grassland biomes Oecologia 155(2)301ndash310DOI 101007s00442-007-0912-y

Hobbie SE Reich PB Oleksyn J Ogdahl M Zytkowiak R Hale C Karolewski P 2006Tree species effects on decomposition and forest floor dynamics in a common gar-den Ecology 87(9)2288ndash2297 DOI 1018900012-9658(2006)87[2288tseoda]20co2

Jiao F Zhong ZM An SS Yuan Z 2013 Successional changes in soil stoichiometry afterland abandonment in Loess Plateau China Ecological Engineering 58(10)249ndash254DOI 101016jecoleng201306036

Jiao JY Zhang ZG BaiWJ Jia YFWang N 2012 Assessing the ecological successof restoration by afforestation on the Chinese Loess Plateau Restoration Ecology20(2)240ndash249 DOI 101111j1526-100X201000756x

John R Dalling JW Harms KE Yavitt JB Stallard RF Mirabello M Hubbell SP Va-lencia R Navarrete H Vallejo M 2007 Soil nutrients influence spatial distributionsof tropical tree species Proceedings of the National Academy of Sciences of the UnitedStates of America 104(3)864ndash869 DOI 101073pnas0604666104

Kang D Guo Y Ren C Zhao F Feng Y Han X Yang G 2014 Population structure andspatial pattern of main tree species in secondary Betula platyphylla forest in ZiwulingMountains China Scientific Reports 41ndash8 DOI 101038srep06873

KoerselmanWMeuleman AFM 1996 The vegetation N P ratio a new tool to detectthe nature of nutrient limitation Journal of Applied Ecology 33(6)1441ndash1450DOI 1023072404783

Ladanai S Aringgren G Olsson B 2010 Relationships between tree and soil propertiesin Picea abies and Pinus sylvestris forests in Sweden Ecosystems 13(2)302ndash316DOI 101007s10021-010-9319-4

Li H Li J He YL Li SJ Liang ZS Peng CH Polle A Luo ZB 2013 Changes in carbonnutrients and stoichiometric relations under different soil depths plant tissues andages in black locust plantations Acta Physiologiae Plantarum 35(10)2951ndash2964DOI 101007s11738-013-1326-6

Liu XZ Dang RY 1993 The study on rational utilization of land resources in hilly andgully areas of Loess Plateau Journal of Soil and Water Conservation 6(2)59ndash67 (inChinese) DOI 1013870jcnkistbcxb199202011

Luuml Y Fu B Feng X Zeng Y Liu Y Chang R Sun GWu B 2012 A policy-drivenlargescale ecological restoration quantifying ecosystem services changes in the LoessPlateau of China PLOS ONE 7(2)e31782 DOI 101371journalpone0031782

Luque GM HochbergME HolyoakM Hossaert M Gaill F Courchamp F2013 Ecological effects of environmental change Ecology Letters Suppl 11ndash3DOI 101111ele12050

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McGroddyME Daufresne T Heedin LO 2004 Scaling of C N P stoichiometryin forests worldwide implications of terrestrial red field-type ratios Ecology85(9)2390ndash2401 DOI 10189003-0351

Nelson JDJ Schoenau JJ Malhi SS 2008 Soil organic carbon changes and distributionin cultivated and restored grassland soils in Saskatchewan Nutrient Cycling inAgroecosystems 82137ndash148 DOI 101007s10705-008-9175-1

Pan FJ ZhangWWang KL He XY Liang SCWei GF 2011 Litter CNP ecological sto-ichiometry character of plant communities in typical karst peak-cluster depressionActa Ecologica Sinica 31(2)335ndash343 (in Chinese) DOI 101002etc434

Parfitt RL Yeates GW Ross DJ 2005 Relationships between soil biota nitrogen andphosphorus availability and pasture growth under organic and conventionalmanagement Applied Soil Ecology 28(1)1ndash13 DOI 101016japsoil200407001

Qi Y Yang F Shukla MK Pu J Chang Q ChuW 2015 Desert soil properties after thirtyyears of vegetation restoration in northern shaanxi province of china Arid LandResearch and Management 29(4)454ndash472 DOI 1010801532498220151030799

Reich PB Oleksyn J 2004 Global patterns of plant leaf N and P in relation to tempera-ture and latitude Proceedings of the National Academy of Sciences of the United Statesof America 101(30)11001ndash11006 DOI 101073pnas0403588101

Sauer TJ James DE Cambardella CA Hernandez-Ramirez G 2012 Soil propertiesfollowing reforestation or afforestation of marginal cropland Plant Soil 360(1ndash2)375ndash390 DOI 101007s11104-012-1258-8

Schreeg LA Santiago LSWright SJ Turner BL 2014 Stem root and older leaf N Pratios are more responsive indicators of soil nutrient availability than new foliageEcology 95(8)2062ndash2068 DOI 10189013-16711

Tang KL Zheng Z Zhang KWang B Cai QWangW 1993 Research methods onrelationship between soil erosion and ecoenvironment in the Ziwuling forest areaMemoir of Northwestern Institute of Soil and Water Conservation Chinese Academy ofSciences 173ndash10 (in Chinese)

Tian HQ Chen GS Zhang C Charles ASH Jerry MM 2010 Pattern and variationof CNP ratios in Chinarsquos soils A synthesis of observational data Biogeochemistry98(1)139ndash151 DOI 101007s10533-009-9382-0

USDANRCS 1999 Soil taxonomy a basic system of soil classification for makingand interpreting soil surveys In [M]Agricultural handbook 436 2nd editionWashington DC US Government Printing Office

Wang HF Lencinas M Ross FCWang XK Qiu JX 2011 Understory plant diversityassessment of Eucalyptus plantations over three vegetation types in Yunnan ChinaNew Forest 42(1)101ndash116 DOI 101007s11056-010-9240-x

Wang KB Shao RX Shangguan ZP 2010 Changes in species richness and communityproductivity during succession on the Loess Plateau of China Polish Journal ofEcology 58(3)549ndash558 DOI 101016jpolar200911001

WarrenMW Zou X 2002 Soil macrofauna and litter nutrients in three tropical treeplantations on a disturbed site in Puerto Rico Forest Ecology and Management170161ndash171 DOI 101016s0378-1127(01)00770-8

Wang and Zheng (2020) PeerJ DOI 107717peerj10084 2021

Wei XR ShaoMA Fu XL Horton R Li Y Zhang XC 2009 Distribution of soil organicC N and P in three adjacent land use patterns in the northern Loess Plateau ChinaBiogeochemistry 96(1ndash3)149ndash162 DOI 101007s10533-009-9350-8

Wright IJ Reich PBWestobyM Ackerly DD Baruch Z Bongers F Cavender-BaresJ Chapin T Cornelissen JH DiemerM Flexas J Garnier E Groom PK Gulias JHikosaka K Lamont BB Lee T LeeW Lusk C Midgley JJ Navas ML NiinemetsU Oleksyn J Osada N Poorter H Poot P Prior L Pyankov VI Roumet C ThomasSC Tjoelker MG Veneklaas EJ Villar R 2004 The worldwide leaf economicsspectrum Nature 428(6985)821ndash827 DOI 101038nature02403

WuTG YuMKWang GG Dong Y Chen XR 2012 Leaf nitrogen and phosphorusstoichiometry across forty-two woody species in Southeast China BiochemicalSystematics and Ecology 44(10)255ndash263 DOI 101016jbse201206002

YuQ Chen QS Elser JJ He NPWuHH Zhang GMWu JG Bai YF Han XG 2010Linking stoichiometric homoeostasis with ecosystem structure functioning andstability Ecology Letters 13(11)1390ndash1399 DOI 101111j1461-0248201001532x

Zeng QC Li X Dong YH An SS Darboux F 2016 Soil and plant components ecologicalstoichiometry in four steppe communities in the Loess Plateau of China Catena147481ndash488 DOI 101016jcatena201607047

Zeng QC Liu Y Fang Y RentianM Rattan L An SS Huang YM 2017 Im-pact of vegetation restoration on plants and soil C N P stoichiometry onthe Yunwu Mountain Reserve of China Ecological Engineering 10992ndash100DOI 101016jecoleng201710003

Zhao FZ Di K Han XH Yang GH Feng YZ Ren GX 2015 Soil stoichiometry andcarbon storage in long-term afforestation soil affected by understory vegetationdiversity Ecological Engineering 74415ndash422 DOI 101016jecoleng201411010

Zhao FZ Zhang L Sun J Ren CJ Han XH Yang GH Pang GW Bai HYWang J 2017Effect of soil C N and P stoichiometry on soil organic C fractions after afforestationPedosphere 27(4)705ndash713 DOI 101016S1002-0160(17)60479-X

Zheng FL 2006 Effect of vegetation changes on soil erosion on the Loess PlateauPedosphere 16(4)420ndash427 DOI 101016S1002-0160(06)60071-4

Zheng SX Shangguan ZP 2007 Spatial patterns of leaf nutrient traits of the plants in theLoess Plateau of China Trees 21(3)357ndash370 DOI 101007s00468-007-0129-z

Zhang YW Shangguan ZP 2016 The coupling interaction of soil water and organiccarbon storage in the long vegetation restoration on the Loess Plateau EcologicalEngineering 91574ndash581 DOI 101016jecoleng201603033

Zhang KL Tang KL 1992 The history of shallow gully development and steep slopereclamation Journal of Soil and Water Conservation 6(2)59ndash67 (in Chinese)DOI 1013870jcnkistbcxb199202011

Zheng FL Tang KL Zhang K Cha X Bai H 1997 Relationship of eco-environmentalchange with natural erosion and artificially accelerated erosion The Journal of ChinaGeography 7(2)75ndash84 (in Chinese)

Wang and Zheng (2020) PeerJ DOI 107717peerj10084 2121