Simin Liu?Hao Wang

Introduction

The mineral status of plants is directly related to their growth and productivity.It is controlled by their genetically fi xed nutrient uptake potential,the nutrient availability in the soil,and other environmental factors(Cernusak et al.2010).Stand ages,soil variability,and changes in slope,elevation,topographic position,and climate interact to affect the mineral nutrition of trees.The complexity and site speci fi city of such interactions is probably the reason why the mineral nutrition of forest trees is still poorly understood.Therefore,it is not yet clear which of the environmental factors in forest ecosystems controls the nutrition of trees.Similarly,very little information is available on the relative amounts of nutrients taken up from the soil by forest trees.

Previous studies have reported that the mineral nutrient concentration in each component(leaf,stem,branch,and root)of forest trees varies widely due to stand age and environmental conditions,particularly heterogeneous soil properties(Masunaga et al.1998a;Domínguez et al.2010;You et al.2013).Vitousek and Sanford(1986)found that nutrient concentrations in individual components of forest trees are more likely to re fl ect the in fl uence of soil fertility.They added that,where a single species is found on two soils that differ in soil fertility,nutrient concentrations in individual components are usually quite similar.

Grubb(1977)observed that mountain forest trees are generally adapted to a relatively poor supply of N and P and thus,tend to have low concentrations of these mineral nutrients.Masunaga et al.(1998a,b)provided new insights into the nutrient characteristics of tropical rain forest trees although they did not relate these to the environmental conditions.The study found that concentrations of most elements were higher in the leaves than in the bark.The authors were also able to classify the trees as accumulators or excluders based on a novel statistical method they employed.In conclusion,among other things,differences in stand age result in wide variations in the nutritional characteristics of trees.In the literature,we could not fi nd similar studies that relate the nutrient status of the trees to environmental factors.

Information on the mineral nutrition of temperate coniferous forest tree species is necessary for understanding the response of forest ecosystems to natural and anthropogenic perturbations,the selection of suitable native reforestation species of degraded areas,and sustainable forest management.Franzaring et al.(2010)found that mineral nutrition is the most important factor limiting the early growth of indigenous forest trees on degraded soils,which underscores the need for more information on the mineral nutrition of native tree species to enhance the use of such trees for the purpose of reforestation.

The objectives of this paper were to evaluate the nutrient status of the dominant tree species in the temperate coniferous forest of northwestern China and to determine its relationship with stand age and environmental factors such as elevation,slope,landscape position,soil pH and soil available nutrients.

Materials and methods

Study site

The study site is located on Qilian Mountain,northwestern China.Three forest districts were selected according to different stand ages and tree species(Fig.1).The sites were chosen because they were relatively undisturbed with no observable anthropogenic in fl uence and because of their landscape diversity and varying stand ages.

Within the elevation range of 2100–3000 m,high vegetation biodiversity exists,indicating a phenomenon of vegetation(Franzaring et al.2010;Li et al.2012).Soils in these sites are arsenic and organic,according to the IUSS Working Group WRB(2006).Climatic data collected from May 2011 to October 2013 from four meteorological stations at altitudes of 1500,2100,2400,and 3000 m showed obvious differences in temperature and precipitation at these four elevations.They also showed a range in annual rainfall from 368.5 mm to 800 mm and a range in mean air temperature from 0.5 to 12.5°C.More detailed information on the forest status is presented in Table 1.

Collection of plant tissue and soil samples

According to different stand ages(young 10–20 a,middleage 20–30 a,mature 30–40 a)and tree species(Picea crassifolia,Pinus armandii,Pinus tabuliformis),29 plots were set in the three forest regions with an area of 25 m×25 m.The subplots(sampling plots)were distributed as follows:9 in the Diebu forest region(34°01′N,103°16′E),10 in the Xiaolongshan Mountains(34°47′N,106°23′E),and 10 in the Qilian Mountains(38°32′N,100°15′E).

Based on the method of scaling for each tree,we chose more than 2 cm in DBH and determination of DBH,tree height,crown width,and height under branch in the sample plot.Combined with the growth factor in the sample plot,we selected three standard sample trees to sample leaves,branches,trunks,roots.Annual leaves and perennial leaves were sampled and then fully mixed.Annual branches and perennial branches were sampled and then fully mixed.The dry samples of trunks were sampled at each 2 m.At each soil layer(20 cm divided 1 layers)we dug up all the roots,which include rootstock,coarse root(DR＞2.0 cm),middle root(1.0 cm＜DR≤2.0 cm),rootlet(0.5 cm＜DR≤1.0 cm),and fi brous roots(DR≤0.5 cm).We then determined the fresh weight of the samples,and crushed,bottled,and labelled the samples.

We measured N,P,K in the soil by pro fi ling,according to each layer at 0–10,10–20,20–40,40–60,and 60–80 cm.We also used strati fi ed sampling:at each layer,three replicate samples of soil were taken,from which N,P,K values were measured.All plant tissue and soil samples were carried out from May 2013 to October 2013.This work was conducted,based on the following forestry standard,‘Observation Methodology for Long-term Forest Ecosystem Research’of the People′s Republic of China.

Chemical analysis

Elemental concentrations of powdered leaf and wood samples were measured after wet digestion,using an H2O2/H2SO4mixture(Jones Jr et al.1990)and atomic absorption spectrophotometry(AAS)for K;an auto sampler(Kjeltec auto sampler 1035 analyzer,Tecator)for N;and photometry for P after color development,following the molybdenum blue method(Murphy and Riley 1962).

Soil properties were analyzed following the USDANRCS methodsas follows:soil pH by applying the potentiometric method to soil–water and soil-KCl solution mixtures in a ratio of 1:1;organic C by the modi fi ed Walkley–Black method;exchangeable K by extraction with 1 M ammonium acetate(pH 7.0)and determined by AAS(Hitachi,180-30 type);and available N by extractionwith 4 M KCl following incubation at 40°C for 7 days and then determined using the Kjeltec Autosampler System 1035 Analyzer;and available P and K by the Bray No.1 and the Mehlich No.1 methods,respectively(Soil Survey Laboratory Staff 1996).

Fig.1 Geographical location of the long-term ecological research site in northwestern China

Table 1 The structural characteristics of vegetation at the different study sites

Statistical analysis

One-way ANOVA was performed to examine the differences in the investigated variables among forests,ecosystem components,and growth strategy.Pearson’s correlation coef fi cients were calculated between the nutrient concentration of each component and the environmental factors.All analyses were conducted using SPSS Statistics 18.0 for Windows.Statistically signi fi cant differences were set at apvalue of 0.05 unless otherwise stated.

The distribution pattern and concentration of mineral nutrients in the trees

We focused on the leaf,branch,stem,and root nutrient concentrations.Figure 2 shows the distribution of leaf,branch,stem,and root concentrations ofP.tabulaeformis,P.armandiiandP.crassifolia(we calculated the weighted average of the 3 stand ages).The results showed that the nutrient concentrations ofP.tabulaeformisleaf,stem,and root were K＞N＞P,and those in the branch were N＞K＞P;forP.armandii,leaf,branch and root,we had N＞K＞P,and stem was N＞K＞P;and forP.crassifolia,leaf,stem and root,we had N＞K＞P,and branch was N＞K＞P.

In general,among the macronutrients,P exhibited the lowest and narrowest concentration in each component(0.039–0.28 g kg-1,mean=0.12),whereas N exhibited the highest(0.095–1.72 g kg-1,mean=0.51).Among components,the leaves had the highest mineral nutrient concentration,and the order of the nutrient concentrations was leaf(0.54 g kg-1)＞branch(0.32 g kg-1)＞root(0.21 g kg-1)＞stem(0.14 g kg-1).P.armandii(0.45 g kg-1)had a higher nutrient concentration thanP.tabulaeformis(0.19 g kg-1) andP.crassifolia(0.29 g kg-1).

Concentration of mineral nutrients in different aged stand

Figure 3 shows statistical analysis of N,P,K content changes ofP.tabulaeformis,P.armandiiandP.crassifoliain different ages.ForP.tabulaeformis:(1)the N,P content of leaves increased fi rst and then decreased from the young forest to the mature forest,The N,P content of the middleage forest was highest,but K content of leaves decreased from the young forest to mature forest;(2)the N,P,K content of branches increased fi rst and then decreased from the young forest to mature forest,the N,P,K content of mature forest was lowest;(3)the N,K content of stems decreased fi rst and then increased from the young forest to mature forest,the N,K content of middle-age forest was lowest,P had no obvious change;(4)the N content of roots increased from the young forest to mature forest,and the P,K content of roots increased fi rst and then decreased from the young forest to mature forest.

ForP.armandiiandP.crassifolia,N,P,K content change trend were similar in the young forest,middle-age forest,and mature forest.The N,P,K content increased fi rst and then decreased from the young forest to mature forest,the N,P,K content of middle-age forest was highest.Figure 3 also showed that the leaves exhibited higher nutrient concentrations than the other components for the three species,P concentration were lower those of than N and K for each component in the different aged stands.

Figure 4 showed the average nutrient concentration of each component in the different aged stands.The order of N,P and K concentrations of the three tree species was middle-age＞young＞mature.The order of total nutrient concentration(N+P+K)of the different stand ages was also middle-age＞young＞mature.

Relationship between nutrient concentrations of trees and environmental factors

Fig.2 Nutrient concentrations distribution of leaf,branch,stem and root of P.tabulaeformis,P.armandii and P.crassifolia.Values=mean±SD(P.tabulaeformis,n=90;P.armandii,n=120;P.crassifolia,n=200)

Fig.3 Nutrient concentrations in each component of different age groups.a–d Leaf,branch,stem and root of P.tabulaeformis;e–h leaf,branch,stem and root of P.armandii;i–l leaf,branch,stem and root of P.crassifolia

Fig.4 Average nutrient concentration in different age groups of studied plant species

The environmental factors that we evaluated included slope,elevation,vegetation type,and soil nutrient status of the 0–10,10–20,20–40,40–60,and 60–80 cm layers in the A horizon,such as organic carbon,and available N,P,and K.Our data for the 5 soil depths revealed very similar relationships between these variables and the nutrient concentrations of each component,apparently due to very similar values of pH and nutrients across these 5 soil depths(Table 2).Hence,for the discussion,we placed emphasis on the fi rst soil depth(0–10 cm)only.It can also be seen in Table 2 that the soil at the study site is weakly basic and contains relatively high mineral nutrient concentrations.

Table 3 shows the Pearson’s correlation coef fi cients between the leaf,branch,stem,and root-nutrient concentrations and the environmental factors.Basically,it showed a negative association between the N,P,and K concentrations of each component and each item.Foliar N,P,and K were negatively correlated(p＜0.001)with available soil N,P,and K,respectively,while no relationships were found between the foliar nutrients and the slope.There wasa signi fi cant(p＜0.001)negative association between branch N and soil N,branch P and soil P(p＜0.05),as well as branch K and soil K(p＜0.01).Stem P and K were negatively correlated(p＜0.001)with elevation and soil K,respectively.Root N,P,and K were negatively correlated(p＜0.001)with elevation,and soil pH had a strong impact on the nutrient concentration in the roots.The soil available nutrients also affected the root nutrients.

Table 2 Average values of soil pH and nutrient status of the study sites(P.tabulaeformis was used as an example)

Table 3 Pearson correlation coef fi cients between nutrient concentration and environmental factors(P.tabulaeformis was used as an example)

Discussion

We collected leaf,stem,branch,and root samples for nutrient analysis.Our results indicated that the analysis of each component was good,showed correlations with the nutrient concentrations in each component as well as with the environmental factors.This con fl icts with reports on the value of foliar analysis for the assessment of the nutritional status of forest trees(He et al.2008;Gartzia-Bengoetxea et al.2009).Some authors considered that the leaf is the focal point of many plant functions and is a relatively sensitive indicator of mineral nutrient status(Hessen et al.2007).Our results suggested that data on nutrient accumulation in plant components,including the leaf,branch,stem and root,can be useful in comparing nutrient status between different species and soils.

Comparing the mean values of the nutrient concentrations measured in this study with those reported for other temperate coniferous forests(Kang et al.2011;Mediavilla et al.2011)indicates that our values are in close agreement,especially with those of generally comparable geology and soil conditions.This implies that it is possible to compare the nutrient status of temperate coniferous forests with comparable environmental conditions despite considerable differences in species composition.This will allow the establishment of optimal and de fi cient levels of nutrients for temperate,coniferous forest stands,which were not clearly delineated until now(Michopoulos et al.2007;Minocha et al.2010;Li et al.2014).

The tendency for foliar nutrient concentrations in most tree species to occur at the higher end of their observed ranges can be ascribed to the low fertility of the soil,implying that soil directly in fl uences the nutrient concentrations of the trees.This also suggests that plants are able to depend on the high nutrient status of the soil by absorbing more nutrients.Chapin(1980)reported that slow-growing wild plant species,characteristic of low fertility soils,usually exhibit low nutrient absorption.

Temperate coniferous forests on low fertile sites have low nutrient concentrations and nutrient cycling ef fi ciency associated with nutrient limitations in forest ecosystems(Chapin 1980).Ecologists consider that low nutrient concentration in temperate coniferous forests is a defense mechanism to prevent the destruction of herbivores;it has recently been found that the frequency of this destruction was still high in temperate coniferous forests ecosystems(Chávez and Macdonald 2010).

The leaves of all three species had higher nutrient concentrations compared with the other plant components,and the leaves are the focal point of many plant functions and are also an accumulator organ.Wu et al.(2007)grouped tree species and organs into accumulators and excluders based on their nutrient status.Those with the ability to absorb relatively high amounts of nutrients are called accumulator species or organs.They found that the leaf and root are accumulator organs.

Grubb(1977)suggested that the selective uptake system in plant roots has a greater effect than leaf anatomy on the concentration of several mineral elements.On the other hand,the genusHelicia,with a very low concentration of nutrients,may be tolerant of such site conditions and are thus considered to be good species for reforestation.The absorption mechanisms of these tree species(those that can absorb high amounts and those that absorb very little)are scienti fi cally interesting and deserve further study.

The order of total nutrient concentration(N+P+K)in the different stand ages was the following:midage＞young＞mature,which is in accordance with natural laws.The middle-age forest is a vigorous growth period:the physiological function and nutrients absorptive capacity are very strong,so they need a lot of nutrient elements in soil t to meet the needs for their normal growth(Sariyildiz and Anderson 2005).The young forest is undergoing development,vitality is low,there is poor resistance to outside conditions,environmental factors affect normal growth,leading to poor soil nutrient absorption and insuf fi cient utilization(Vitousek et al.2010;Yu and Sun 2013).As forests mature,the result is poor physiological function digestion and poor absorption ability.Their absorption utilization rate is low to soil nutrient,so their nutrient content are low(Zhang et al.2012).

The very low concentration of P in the trees may be attributed to the low P availability in the soil.However,the narrow concentration range in the trees implies low nutrient absorption and requirement by the forest trees regardless of species.P is known to be the most limiting nutrient in many forest soils(Susaya and Asio 2005)and has been hypothesized to limit the productivity of forests(Wardle et al.2004).Our results tend to support this hypothesis.

The effects of geomorphic factors are interrelated,and it is dif fi cult to isolate these factors.Slope is also related since it varies with topographic position.The variation in geomorphic factors results in considerable variation in soil properties and nutrient status.It is likely that vegetation differs in terms of composition at different elevations in response to these variations in environmental conditions(Webb and Donoghue 2005).Nevertheless,it appears that topographic position,vegetation type and soil nutrient status had the greatest effect on the nutrient concentration of the trees.The latter factor,however,was only true for some nutrients.

Conclusions

The P content in three species was the lowest,while N content was the highest.The nutrient content of leaves was the highest and the total nutrient elements of each organ were as follows:leaf＞branch＞root＞stem.From the young forest to mature forest,ForP.tabulaeformis,the N,P content of leaves,the N,P,K content of branches and the P,K content of roots increased fi rst and then decreased;the N,K content of stems decreased fi rst and then increased;and P had no obvious change.The N content of roots increased from the young forest to the mature forest.ForP.armandiiandP.crassifolia,the N,P,K content increased fi rst and then decreased from the young forest to mature forest.Overall,P.armandiihad a higher nutrient concentration thanP.tabulaeformisandP.crassifolia.The nutrient content of each species is highest in the young forest,but lowest in the mature forest.The nutrient content of each tree species was signi fi cantly affected by soil nutrient content,and negatively correlated with soil-available nutrients.In addition,elevation and soil pH had a greater effect on root and dry nutrients.

AcknowledgementsWe appreciated the reviewer’s comments on the previous version of the manuscript,which helped us greatly improve the quality and readability of the paper.

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