鼎湖山森林演替序列植物-土壤碳氮同位素特征

doi:10.17521/cjpe.2015.0478

摘要/Abstract

摘要：

植物群落对水分利用和养分利用的优化策略, 土壤碳周转和氮循环过程对演替变化如何响应, 森林土壤有机碳积累机制等都是森林生态学需要解决的关键问题。然而, 这些生态学过程的变化在短时间内通过传统的研究手段难以被精确观测, 碳氮同位素(¹³C、¹⁵N)技术的应用或许能提供更多有价值的信息。该文通过对鼎湖山森林演替序列代表性群落——马尾松(Pinus massoniana)针叶林(PF)、针阔叶混交林(MF)和季风常绿阔叶林(BF)植物-土壤碳氮同位素自然丰度的测定, 分析了叶片稳定碳同位素比率(δ¹³C)和稳定氮同位素比率(δ¹⁵N)与其叶片元素含量的关系, 以及叶片-凋落物-土壤δ¹³C、δ¹⁵N在演替水平和垂直方向上的变化特征。结果显示: 1)主要优势树种叶片δ¹³C与其C:N极显著正相关(p < 0.01), 凋落物和各层土壤δ¹³C均表现为PF > MF > BF, 沿演替方向逐渐降低; 2)叶片δ¹⁵N与叶片N含量正相关(p = 0.05), 凋落物和表层土壤(0-10 cm) δ¹⁵N沿演替方向逐渐增大; 3)不同演替阶段土壤δ¹³C、δ¹⁵N均沿垂直剖面呈现增大的趋势。结果表明: 南亚热带地区植物群落的发展并不一定受水分利用和氮素利用的补偿制约; δ¹³C自然丰度法的应用有助于森林土壤有机碳积累机制, 尤其有助于成熟森林土壤“碳汇”机制的阐释; 植物-土壤δ¹⁵N值可作为评估土壤氮素有效性和生态系统“氮饱和”状态的潜在指标。

关键词: 稳定碳同位素比率, 稳定氮同位素比率, 演替, 森林, 鼎湖山

Abstract:

Aims The optimal patterns of plant community for water use and nutrient utilization, the responses of soil carbon and nitrogen turnover processes to forest succession, and the mechanisms of soil organic carbon accumulation, are three critical issues in forest ecosystem study. It is difficult to accurately detect these ecological processes with conventional methodologies in the short term, yet the application of ¹³C and ¹⁵N natural abundance technique may yield important information about these processes.Methods This study was conducted in Dinghushan Biosphere Reserve. We investigated the natural isotopic abundance of both ¹³C and ¹⁵N of plant-soil continuum along a successional gradient from Pinus massoniana forest (PF) to coniferous and broad-leaved mixed forest (MF), and monsoon evergreen broad-leaved forest (BF). We also analyzed the correlations of foliar stable carbon isotope ratio (δ¹³C) and stable nitrogen isotope ratio (δ¹⁵N) with foliar elemental contents and the variations of soil δ¹³C and δ¹⁵N along soil profiles at different successional stages.Important findings A significant positive correlation between foliar δ¹³C and foliar C:N was observed. In both litter and soil, the δ¹³C values tended to decrease along the forest succession, with the order as PF > MF > BF. Foliar δ¹⁵N was positively correlated with foliar N content. The δ¹⁵N values of litter and upper soil (0-10 cm) increased with successional status. Both soil δ¹³C and δ¹⁵N values increased with increasing soil depth at all three forests. Our results imply that 1) trade-off between water use efficiency and nitrogen use efficiency did not necessarily exist in subtropical forests of China; 2) the application of isotopic technique could assist understanding of the mechanisms of soil carbon accumulation in subtropical forests, especially in old-grow forests; 3) the ¹⁵N natural abundance of plant-soil continuum could be a potential indicator of soil nitrogen availability and ecosystem nitrogen saturation status.

Key words: stable carbon isotope ratio, stable nitrogen isotope ratio, succession, forest, Dinghushan

熊鑫, 张慧玲, 吴建平, 褚国伟, 周国逸, 张德强. 鼎湖山森林演替序列植物-土壤碳氮同位素特征. 植物生态学报, 2016, 40(6): 533-542. DOI: 10.17521/cjpe.2015.0478

Xin XIONG, Hui-Ling ZHANG, Jian-Ping WU, Guo-Wei CHU, Guo-Yi ZHOU, De-Qiang ZHANG. ¹³C and ¹⁵N isotopic signatures of plant-soil continuum along a successional gradient in Dinghushan Biosphere Reserve. Chinese Journal of Plant Ecology, 2016, 40(6): 533-542. DOI: 10.17521/cjpe.2015.0478

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链接本文: https://www.plant-ecology.com/CN/10.17521/cjpe.2015.0478

https://www.plant-ecology.com/CN/Y2016/V40/I6/533

图/表 6

表1 共有优势种叶片稳定碳、氮同位素比率在不同林型间的差异

Table 1 Differences in foliar carbon isotope ratio (δ13C) and nitrogen isotope ratio (δ15N) of common dominant species among different forest types

共有树种 Common species	林型 Forest type	稳定碳同位素比率 δ¹³C (‰)	稳定氮同位素比率 δ¹⁵N (‰)
马尾松 Pinus massoniana	松林 Pine forest	-29.28 (0.19)	-5.15 (0.24)
马尾松 Pinus massoniana	混交林 Mixed forest	-30.30 (0.10)^**	-4.07 (0.11)^*
木荷 Schima superba	混交林 Mixed forest	-30.77 (0.53)	-3.56 (0.18)
木荷 Schima superba	阔叶林 Broad-leaved forest	-29.19 (0.69)	-5.41 (0.09)^**
锥 Castanopsis chinensis	混交林 Mixed forest	-30.90 (0.21)	-2.73 (0.41)
锥 Castanopsis chinensis	阔叶林 Broad-leaved forest	-29.88 (0.79)	-3.09 (0.57)
厚壳桂 Cryptocarya chinensis	混交林 Mixed forest	-33.37 (0.12)	-3.75 (0.21)
厚壳桂 Cryptocarya chinensis	阔叶林 Broad-leaved forest	-32.94 (0.35)	-3.59 (0.40)

图1 叶片稳定碳(C)、氮(N)同位素比率与元素含量的关系。

Fig. 1 Correlations of foliar stable carbon isotope ratio (δ13C) and stable nitrogen isotope ratio (δ15N) with foliar elemental contents.

表2 不同林型凋落物稳定碳、氮同位素比率与碳氮比

Table 2 The stable carbon isotope ratio (δ13C) and stable nitrogen isotope ratio (δ15N) and the C:N of the litter from different forest types

林型 Forest type	稳定碳同位素比率 δ¹³C (‰)	稳定氮同位素比率 δ¹⁵N (‰)	碳氮比 C:N
松林 Pine forest	-28.84 (0.09)^a	-5.19 (0.08)^b	46.11 (0.63)^a
混交林 Mixed forest	-29.78 (0.04)^b	-4.40 (0.06)^ab	41.39 (0.42)^b
阔叶林 Broad-leaved forest	-30.43 (0.19)^c	-4.02 (0.52)^a	31.73 (1.87)^c

表3 土壤稳定碳、氮同位素比率和元素含量的方差分析结果

Table 3 Effects of forest type, soil layer and and their interaction on soil stable carbon isotope ratio (δ13C), stable nitrogen isotope ratio (δ15N), total organic carbon (TOC), readily oxidized organic carbon content (ROC), microbial biomass carbon content (MBC), total nitrogen content (TN) and the C to N ratio (C:N)

主效应和交互作用 Main effect or interaction	因变量 Dependent variable
主效应和交互作用 Main effect or interaction	稳定碳同位素比率 δ¹³C	稳定氮同位素比率 δ¹⁵N	土壤总有机碳生物 TOC	易氧化有机碳含量 ROC	微生物生物量碳含量 MBC	总氮含量 TN	碳氮比 C:N
林型 Forest type	F₂= 96.39^**	F₂= 2.02	F₂= 54.74^**	F₂= 24.81^**	F₂= 15.34^**	F₂= 92.32^**	F₂ = 25.77^**
土层 Soil layer	F₃= 53.77^**	F₃= 133.56^**	F₃= 233.24^**	F₃= 244.47^**	F₃= 23.74^**	F₃= 232.26^**	F₃= 162.36^**
林型×土层 Forest type × soil layer	F₁₁= 3.00^**	F₁₁= 1.65	F₁₁= 7.47^**	F₁₁= 4.62^**	F₁₁= 1.83	F₁₁= 6.99^**	F₁₁= 4.90^**

图2 土壤稳定碳同位素比率(A)、总有机碳含量TOC (B)、稳定氮同位素比率(C)、总氮含量TN (D)沿剖面变化特征(平均值±标准误差)。BF, 阔叶林; MF, 混交林; PF, 松林。

Fig. 2 Distribution characteristics of soil stable carbon isotope ratio (δ13C, A) and total organic carbon content (TOC, B) and stable nitrogen isotope ratio (δ15N, C) and total nitrogen content (TN, D) along soil profiles (mean ± SE). BF, broad-leaved forest; MF, mixed forest; PF, pine forest.

图3 不同林型各土层易氧化有机碳含量(ROC, A)、微生物生物量碳含量(MBC, B)和碳氮比(C:N, C)的变化(平均值±标准误差)。不同字母表示同一土层不同林型间差异显著(p < 0.05)。PF, 松林; MF, 混交林; BF, 阔叶林。

Fig. 3 Change of readily oxidized organic carbon content (ROC, A) and microbial biomass carbon content (MBC, B) and the C to N ratio (C:N, C) at different soil layers under different forests (mean ± SE). Different letters indicate significant differences among forests for the same soil layer at p < 0.05. BF, broad-leaved forest; MF, mixed forest; PF, pine forest.

参考文献 46

1	Balesdent J, Girardin C, Mariotti A (1993). Site-related δ13C of tree leaves and soil organic matter in a temperate forest.Ecology, 74, 1713-1721.
2	Bernoux M, Cerri CC, Neill C, Moraes JFL (1998). The use of stable carbon isotopes for estimating soil organic matter turnover rates.Geoderma, 82, 43-58.
3	Blair GJ, Lefroy RDB, Lisle L (1995). Soil carbon fractions based on their degree of oxidation and the development of a carbon management index for agricultural systems.Aus- tralian Journal of Agricultural Research, 46, 1459-1466.
4	Cernusak LA, Ubierna N, Winter K, Holtum JAM, Marshall JD, Farquhar GD (2013). Environmental and physiological determinants of carbon isotope discrimination in terrestrial plants.New Phytologist, 200, 950-965.
5	Chen H, Gurmesa GA, Zhang W, Zhu XM, Zheng MH, Mao QG, Zhang T, Mo JM (2015). Nitrogen saturation in humid tropical forests after 6 years of nitrogen and phosphorus addition: Hypothesis testing.Functional Ecology, 17(2), 59-73.
6	Chen QQ, Shen CD, Peng SL, Yi WX, Sun YM, Li ZA, Jiang MT (2002). Characteristics and controlling factors of soil organic matter turnover processes in the subtropical mountainous area, South China.Acta Ecologica Sinica, 22, 1446-1454. (in Chinese with English abstract)[陈庆强, 沈承德, 彭少麟, 易惟熙, 孙彦敏, 李志安, 姜漫涛 (2002). 华南亚热带山地土壤有机质更新特征及其影响因子. 生态学报, 22, 1446-1454.]
7	Chen SP, Bai YF, Zhang LX, Han XG (2005). Comparing physiological responses of two dominant grass species to nitrogen addition in Xilin River Basin of China.Environmental and Experimental Botany, 53, 65-75.
8	Cheng XL, Yang YH, Li M, Dou XL, Zhang QF (2013). The impact of agricultural land use changes on soil organic carbon dynamics in the Danjiangkou Reservior area of China.Plant and Soil, 366, 415-424.
9	Craine JM, Elmore AJ, Aidar MPM, Bustamante M, Dawson TE, Hobbie EA (2009). Global patterns of foliar nitrogen isotopes and their relationships with climate, mycorrhizal fungi, foliar nutrient concentrations, and nitrogen availability.New Phytologist, 183, 980-992.
10	Ehleringer JR, Buchmann N, Flanagan LB (2000). Carbon isotope ratios in belowground carbon cycle processes.Ecological Applications, 10, 412-422.
11	Ehleringer JR, Lin ZF, Field CB, Kuo CY (1986). Leaf carbon isotope ratio and mineral composition in subtropical plants along an irradiance cline.Oecologia, 72, 109-114.
12	Falkengren-Grerup U, Michelsen A, Olsson MO, Quarmby C, Sleep D (2004). Plant nitrate use in deciduous woodland: The relationship between leaf N, 15N natural abundance of forbs and soil N mineralisationmineralization.Soil Biology & Biochemistry, 36, 1885-1891.
13	Farquhar GD, O’Leary MH, Berry JA (1982). On the relationship between carbon isotope discrimination and the inter- cellular carbon dioxide concentration in leaves.Australian Journal of Plant Physiology, 9, 121-137.
14	Field C, Merino J, Mooney HA (1983). Compromises between water-use efficiency and nitrogen-use efficiency in five species of California evergreens.Oecologia, 60, 384-389.
15	Galdo ID, Six J, Peressotti A, Cotrufo MF (2003). Assessing the impact of land-use change on soil sequestration in agriculture soils by means of organic matter fraction and stable C isotopes.Global Change Biology, 9, 1204-1213.
16	Garten CT, Taylor GE (1992). Foliar δ13C within a temperate deciduous forest: Spatial, temporal, and species sources of variation.Oecologia, 90, 1-7.
17	Gleixner G, Danier HJ, Werner RA, Schmidt HL (1993). Correlations between the 13C content of primary and secondary plant products in different cell compartments and that in decomposing Basidiomycetes.Plant Physiology, 102, 1287-1290.
18	Hobbie EA, Macko SA, Williams M (2000). Correlation be- tween foliar δ15N and nitrogen concentrations may indicate plant-mycorrhizal interactions.Oecologia, 122, 273-283.
19	Hobbie EA, Ouimette AP (2009). Controls of nitrogen isotope patterns in soil profiles.Biogeochemistry, 95, 355-371.
20	Hobbie EA, Werner RA (2004). Intramolecular, compound- specific, and bulk carbon isotope patterns in C3 and C4 plants: A review and synthesis.New Phytologist, 161, 371-385.
21	Högberg P (1997). 15N natural abundance in soil-plant systems.New Phytologist, 137, 179-203.
22	Högberg P, Ekblad A (1996). Substrate-induced respiration measured in situ in a C3-plant ecosystem using additions of C4-sucrose.Soil Biology & Biochemistry, 28, 1131-1138.
23	Huang YH, Li YL, Xiao Y, Wenigmann KO, Zhou GY, Zhang DQ, Wenigmann M, Tang XL, Liu JX (2011). Controls of litter quality on the carbon sink in soils through partitioning the products of decomposing litter in a forest succession series in South China.Forest Ecology and Management, 261, 1170-1177.
24	Huang ZL, Kong GH, Zhang QM, Liu SZ (1998). Structure, species diversity and population dynamics of the lower subtropical evergreen broad-leaved forest in Dinghushan Biosphere Reserve.Tropical and Subtropical Forest Ecosystem, 1, 64-75. (in Chinese with English abstract)[黄忠良, 孔国辉, 张倩媚, 刘世忠 (1998). 鼎湖山南亚热带常绿阔叶林结构、物种多样性及种群动态的研究. 热带亚热带森林生态系统研究, 1, 64-75.]
25	Kahmen A, Wanek W, Buchmann N (2008). Foliar δ15N values characterize soil N cycling and reflect nitrate or ammonium preference of plants along a temperate grassland gradient.Oecologia, 156, 861-870.
26	Ledgard SF, Feney JR, Simpson JR (1984). Variations in natural enrichment of 15N in the profiles of some Australian pasture soils.Australian Journal of Soil Research, 22, 155-164.
27	Liao JD, Boutton TW, Jastrow JD (2006). Organic matter turnover in soil physical fractions following woody plant invasion of grassland: Evidence from natural 13C and 15N.Soil Biology & Biochemistry, 38, 3197-3210.
28	Liu XD, Zhou GY, Chen XZ, Zhang DQ, Zhang QM (2014). Forest microclimate change along with the succession and response to climate change in south subtropical region.Acta Ecologica Sinica, 34, 2755-2764. (in Chinese with English abstract)[刘效东, 周国逸, 陈修治, 张德强, 张倩媚 (2014). 南亚热带森林演替过程中小气候的改变及对气候变化的响应. 生态学报, 34, 2755-2764.]
29	Mariotti A, Pierre D, Vedy JC, Bruckert S, Guillemot J (1980). The abundance of natural nitrogen 15 in the organic matter of soils along an altitudinal gradient.Catena, 7, 293-300.
30	Nadelhoffer KJ, Fry B (1988). Controls on natural nitrogen-15 and carbon-13 abundances in forest soil organic matter.Soil Science Society of America Journal, 52, 1633-1640.
31	O’Leary MH (1981). Carbon isotope fractionation in plants.Phytochemistry, 20, 553-567.
32	O’Leary MH (1988). Carbon isotopes in photosynthesis.Bioscience, 38, 328-336.
33	Ouyang X, Li YL, Zhang QM (2014). Characteristics of microclimate in a mixed coniferous and broadleaf forest in Dinghushan Biosphere Reserve.Chinese Journal of Ecology, 33, 575-582. (in Chinese with English abstract)[欧阳旭, 李跃林, 张倩媚 (2014). 鼎湖山针阔叶混交林小气候调节效应. 生态学杂志, 33, 575-582.]
34	Pardo LH, Hemond HF, Montoya JP, Fahey TJ, Siccama TG (2002). Response of the natural abundance of 15N in forest soils and foliage to high nitrate loss following clear cutting.Canadian Journal of Forest Research, 32, 1126-1136.
35	Shearer G, Kohl DH (1986). N2-fixation in field settings: Estimations based on natural 15N abundance.Australian Journal of Plant Physiology, 13, 699-756.
36	Sun GC, Lin ZF, Lin GZ, Li SS (1993). 13C/12C ratio and water use efficiency of Pinus massoniana in subtropical artificial forest.Chinese Journal of Applied Ecology, 4, 325-327. (in Chinese with English abstract)[孙谷畴, 林植芳, 林桂珠, 李双顺 (1993). 亚热带人工林松树13C/12C比率和水分利用效率. 应用生态学报, 4, 325-327.]
37	Tcherkez G, Hodges M (2008). How stable isotopes may help to elucidate primary nitrogen metabolism and its interaction with (photo) respiration in C3 leaves.Journal of Experimental Botany, 59, 941-953.
38	Templer PH, Arthur MA, Lovett GM, Weathers KC (2007). Plant and soil natural abundance δ15N: Indicators of relative rates of nitrogen cycling in temperate forest ecosystems.Oecologia, 153, 399-406.
39	Tiessen H, Karamanos RE, Stewart JWB, Selles F (1984). Natural nitrogen-15 abundance as an indicator of soil organic matter transformations in native and cultivated soils.Soil Science Society of America Journal, 48, 312-315.
40	Tsialtas JT, Handley LL, Kassioumi MT, Veresoglou DS, Gagianas AA (2001). Interspecific variation in potential water use efficiency and its relation to plant species abundance in a water-limited grassland.Functional Ecology, 15, 605-614.
41	Vance ED, Brookes PC, Jenkinson DS (1987). An extraction method for measuring soil microbial biomass C.Soil Biology & Biochemistry, 19, 703-707.
42	Xu YQ, He JC, Cheng WX, Xing XR, Li LH (2010). Natural 15N abundance in soils and plants in relation to N cycling in a rangeland in Inner Mongolia.Journal of Plant Ecology, 3, 201-207.
43	Yu GR, Wang SQ, Chen PQ, Li QK (2005). Isotope tracer approaches in soil organic carbon cycle research.Advances in Earth Science, 20, 568-577. (in Chinese with English abstract)[于贵瑞, 王绍强, 陈泮勤, 李庆康 (2005). 碳同位素技术在土壤碳循环研究中的应用. 地球科学进展, 20, 568-577.]
44	Zhang J, Gu L, Bao F, Cao Y, Hao Y, He J, Li J, Li Y, Ren Y, Wang F, Wu R, Yao B, Zhao Y, Lin G, Wu B, Lu Q, Meng P (2015). Nitrogen control of 13C enrichment in heterotrophic organs relative to leaves in a landscape- building desert plant species.Biogeosciences, 12, 15-27.
45	Zhou GY, Liu SG, Li ZA, Zhang DQ, Tang XL, Zhou CY, Yan JH, Mo JM (2006a). Old-growth forests can accumulate carbon in soils.Science, 314, 1417.
46	Zhou GY, Zhou CY, Liu SG, Tang XL, Ouyang XJ, Zhang DQ, Liu SZ, Liu JX, Yan JH, Wen DZ, Xu GL, Zhou CY, Luo Y, Guan LL, Liu Y (2006b). Belowground carbon balance and carbon accumulation rate in the successional serials of monsoon evergreen broad-leaved forest.Science in China Serial D-Earth Science, 49, 311-321.

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[14]	董涵君, 王兴昌, 苑丹阳, 柳荻, 刘玉龙, 桑英, 王晓春. 温带不同材性树种树干非结构性碳水化合物的径向分配差异[J]. 植物生态学报, 2022, 46(6): 722-734.
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