Chin J Plant Ecol ›› 2019, Vol. 43 ›› Issue (7): 576-584.doi: 10.17521/cjpe.2019.0009

• Research Articles • Previous Articles     Next Articles

13C pulse labeling reveals the effects of grazing on partitioning of assimilated carbon in an alpine meadow

CHEN Jin1,2,SONG Ming-Hua1,*(),LI Yi-Kang3   

  1. 1Key Laboratory of Ecosystem Network Observation and Modeling, Institute of Geographic Sciences and Natural Resources Research, Chinese Academy of Sciences, Beijing 100101, China
    2University of Chinese Academy of Sciences, Beijing 100049, China
    3Northwest Institute of Plateau Biology, Chinese Academy of Sciences, Xining 810008, China
  • Received:2019-01-10 Accepted:2019-06-25 Online:2019-12-12 Published:2019-07-20
  • Contact: SONG Ming-Hua
  • Supported by:
    Supported by the National Key R&D Program of China(2016YFC0502001);Supported by the National Key R&D Program of China(2016YFC0501803);the National Natural Science Foundation of China(41671263)


Aims In this study, we aim to understand how grazing would influence the partitioning of assimilated carbon in an alpine meadow on the Qinghai-Xizang Plateau.
Methods Measurements on carbon partitioning were made in a long-term grazing experiment consisting of light winter grazing and enclosure treatments. The 13C tracer method was used to determine the partitioning and transportation of assimilated carbon into different carbon pools.
Important findings On the 30th day following the labeling, shoots retained 32% of the initial 13C, and roots and soil together retained 22%; about 30% of the initial 13C were lost through shoot respiration. There were significant differences in the retention in soil, and the respiratory emission from soil, of assimilated carbon between the light grazing and enclosure treatments. Under light grazing, plants invested more assimilated carbon into the root and soil carbon pools. The rate of 13C transportation from shoots to soil and the rate of respiratory 13C release from soil were both greater, and the retention of 13C in and respiratory release from shoots were lower, under light grazing than under enclosure. Our results suggest that grazing is an important mechanism for maintenance of grassland. Grazing may cause changes in the structure and functioning of ecosystems, and induce large variations in soil carbon storage. Alpine meadow in the Qinghai-Xizang Plateau is amongst the grasslands with highest elevation in the world, and has large soil carbon storage due to low temperatures. We found no difference in soil C stocks between light grazing and enclosure treatments, indicating that light grazing would have no significant impact on soil carbon stocks.

Key words: grazing, 13C isotope labeling, alpine meadow, partitioning of assimilated carbon

Fig. 1

Carbon (C) stock in soil (A) and plants (B) in light winter grazed (LWG) and fence-enclosed (Encl) alpine meadows and in plant shoot (C) and root (D) (mean ± SE). * indicates significant difference between grazed and ungrazed plots (p < 0.05)."

Fig. 2

Cumulative soil CO2-C efflux over 30 days following 13C labelling in light winter grazed (LWG) and fence-enclosed (Encl) alpine meadows(mean ± SE). * indicates significant difference between grazed and ungrazed plots (p < 0.05)."

Fig. 3

13C dynamics in shoots and roots and 13C losses by shoot respiration during a 30 day period following 13C labelling in light winter grazed (LWG) and fence-enclosed (Encl) alpine meadows (mean ± SE). * indicates significant difference between grazed and ungrazed plots (p < 0.05)."

Fig. 4

13C dynamics in roots and soil during a 30 day period following 13C labelling in light winter grazed (LWG) and fence- enclosed (Encl) alpine meadows (mean ± SE). * indicates significant difference between grazed and ungrazed plots (p < 0.05)."

Fig. 5

13CO2-C efflux rate in soil of light winter grazed (LWG) and fence-enclosed (Encl) alpine meadows during a 30 day period following 13C labelling (mean ± SE). * indicates significant difference between grazed and ungrazed plots (p < 0.05)."

[1] Burenbayin ( 2012). Effect of Different Grazing Seasons on the Plant Diversity and Productivity in Kobresia Alpine Meadow. Master degree dissertation, Chinese Academy of Sciences, Beijing.
[ 布仁巴音 ( 2012). 不同季节放牧对高寒草甸植物群落多样性和生产力的影响. 硕士学位论文, 中国科学院研究生院, 北京.]
[2] Cao GM, Tang YH, Mo WH, Wang YS, Li YN, Zhao XQ ( 2004). Grazing intensity alters soil respiration in an alpine meadow on the Tibetan Plateau. Soil Biology & Biochemistry, 36, 237-243.
doi: 10.1111/gcb.14962 pmid: 31838767
[3] Chinese Soil Taxonomy Research Group ( 1995). Chinese Soil Taxonomy. Science Press, Beijing. 58-147.
[ 中国土壤分类学研究组 ( 1995). 中国土壤分类. 科学出版社, 北京. 58-147.]
[4] Cingolani AM, Noy-Meir I, Díaz S ( 2005). Grazing effects on rangeland diversity: A synthesis of contemporary models. Ecological Applications, 15, 757-773.
doi: 10.1890/03-5272
[5] Doescher PS, Svejcar TJ, Jaindl RG ( 1997). Gas exchange of Idaho fescue in response to defoliation and grazing history. Journal of Range Management, 50, 285-289.
doi: 10.2307/4003731
[6] Gao YH, Zeng XY, Schumann M, Chen H ( 2011). Effectiveness of exclosures on restoration of degraded alpine meadow in the eastern Tibetan Plateau. Arid Land Research and Management, 25, 164-175.
doi: 10.1080/15324982.2011.554954
[7] Gao YZ, Giese M, Lin S, Sattelmacher B, Zhao Y, Brueck H ( 2008). Belowground net primary productivity and biomass allocation of a grassland in Inner Mongolia is affected by grazing intensity. Plant and Soil, 307, 41-50.
doi: 10.1007/s11104-008-9579-3
[8] Haferkamp MR, MacNeil MD ( 2004). Grazing effects on carbon dynamics in the northern mixed-grass prairie. Environmental Management, 3(S1), S462-S474.
[9] Hafner S, Unteregelsbacher S, Seeber E, Lena B, Xu XL, Li XG, Guggenberger G, Miehe G, Kuzyakov Y ( 2012). Effect of grazing on carbon stocks and assimilate partitioning in a Tibetan montane pasture revealed by 13CO2 pulse labeling . Global Change Biology, 18, 528-538.
doi: 10.1111/j.1365-2486.2011.02557.x
[10] Hamblin A, Tennant D, Perry MW ( 1990). The cost of stress: Dry matter partitioning changes with seasonal supply of water and nitrogen to dryland wheat. Plant and Soil, 122, 47-58.
[11] Herzschuh U, Birks HJB, Ni J, Zhao Y, Liu H, Liu X, Grosse G ( 2010). Holocene land-cover changes on the Tibetan Plateau. The Holocene, 20(1), 91-104.
doi: 10.1177/0959683609348882
[12] IPCC ( Intergovernmental Panel on Climate Change) ( 2001). Climate Change 2001: The Scientific Basis. Cambridge University Press, New York, USA. 881.
[13] Klumpp K, Soussana JF ( 2009). Using functional traits to predict grassland ecosystem change: A mathematical test of the response-and-effect trait approach. Global Change Biology, 15, 2921-2934.
doi: 10.1111/gcb.2009.15.issue-12
[14] Kuzyakov Y, Domanski G ( 2000). Carbon input by plants into the soil. Review. Journal of Plant Nutrition and Soil Science, 163, 421-431.
doi: 10.1016/j.tplants.2019.07.008 pmid: 31488354
[15] Lettens S, Orshoven J, Wesemael B, Muys B, Perrin D ( 2005). Soil organic carbon changes in landscape units of Belgium between 1960 and 2000 with reference to 1990. Global Change Biology, 11, 2128-2140.
doi: 10.1111/gcb.2005.11.issue-12
[16] McNaughton SJ ( 1979). Grazing as an optimization process: Grass-ungulate relationships in the Serengeti. The American Naturalist, 113, 691-703.
doi: 10.1086/283426
[17] McNaughton SJ ( 1985). Ecology of a grazing ecosystem: The Serengeti. Ecological Monographs, 55, 259-294.
doi: 10.1111/j.1365-2656.2011.01885.x pmid: 21801174
[18] McNaughton SJ ( 1993). Grasses and grazers, science and management. Ecological Applications, 3, 17-20.
doi: 10.1007/s00442-016-3627-0 pmid: 27094543
[19] McNaughton SJ, Ruess RW, Seagle SW ( 1988). Large mammals and process dynamics in African ecosystems. BioScience, 38, 794-800.
doi: 10.1159/000492998 pmid: 30799412
[20] Menke J, Bradford GE ( 1992). Rangelands. Agriculture, Ecosystems & Environment, 42, 141-163.
doi: 10.1007/s11356-019-06538-4 pmid: 31838703
[21] Milchunas DG, Lauenroth WK ( 1993). Quantitative effects of grazing on vegetation and soils over a global range of environments. Ecological Monographs, 63, 327-366.
doi: 10.2307/2937150
[22] Morris JT, Jensen A ( 1998). The carbon balance of grazed and non-grazed Spartina anglica saltmarshes at Skallingen, Denmark. Journal of Ecology, 86, 229-242.
doi: 10.1046/j.1365-2745.1998.00251.x
[23] Ni J ( 2002). Carbon storage in grasslands of China. Journal of Arid Environments, 50, 205-218.
doi: 10.1371/journal.pone.0225952 pmid: 31805113
[24] Oesterheld M, Loreti J, Semmartin M, Paruelo JM ( 1999). Grazing, fire, and climate effects on primary productivity of grasslands and savannas. In: Walker LR ed. Ecosystems of Disturbed Ground. Elsevier, New York, USA. 287-306.
[25] Rangel-Castro JI, Prosser JI, Scrimgeour CM, Smith P, Ostle N, Ineson P, Meharg A, Killham K ( 2004). Carbon flow in an upland grassland: Effect of liming on the flux of recently photosynthesized carbon to rhizosphere soil. Global Change Biology, 10, 2100-2108.
doi: 10.1111/gcb.2004.10.issue-12
[26] Rogiers N, Eugster W, Furger M, Siegwolf R ( 2005). Effect of land management on ecosystem carbon fluxes at a subalpine grassland site in the Swiss Alps. Theoretical and Applied Climatology, 80, 187-203.
doi: 10.1007/s00704-004-0099-7
[27] Scurlock JMO, Hall DO ( 1998). The global carbon sink: A grassland perspective. Global Change Biology, 4, 229-233.
doi: 10.1016/j.scitotenv.2018.08.140 pmid: 30118941
[28] Song M, Guo Y, Yu F, Zhang X, Cao G, Cornelissen JHC ( 2018). Shifts in priming partly explain impacts of long-term nitrogen input in different chemical forms on soil organic carbon storage. Global Change Biology, 24, 4160-4172.
doi: 10.1111/gcb.14304 pmid: 29748989
[29] Song MH, Yu FH, Ouyang H, Cao GM, Xu XL, Cornelissen JHC ( 2012). Different inter-annual responses to availability and form of nitrogen explain species coexistence in an alpine meadow community after release from grazing. Global Change Biology, 18, 3100-3111.
doi: 10.1111/j.1365-2486.2012.02738.x pmid: 28741827
[30] Sun Y, Xu XL, Kuzyakov Y ( 2014). Mechanisms of rhizosphere priming effects and their ecological significance . Chinese Journal of Plant Ecology, 38, 62-75.
doi: 10.3724/SP.J.1258.2014.00007
[ 孙悦, 徐兴良, KUZYAKOV Yakov ( 2014). 根际激发效应的发生机制及其生态重要性. 植物生态学报, 38, 62-75.]
doi: 10.3724/SP.J.1258.2014.00007
[31] Thomas AD ( 2012). Impact of grazing intensity on seasonal variations in soil organic carbon and soil CO2 efflux in two semiarid grasslands in southern Botswana. Philosophical Transactions of the Royal Society B: Biological Sciences, 367, 3076-3086.
doi: 10.1098/rstb.2012.0102 pmid: 23045706
[32] UNEP ( 1993). Agenda 21 Rio Declaration. United Nations, New York, USA.
[33] Walkley A, Black IA ( 1934). An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Science, 37, 29-38.
doi: 10.1097/00010694-193401000-00003
[34] Ward SE, Bardgett RD, McNamara NP, Adamson JK, Ostle NJ ( 2007). Long-term consequences of grazing and burning on northern peatland carbon dynamics. Ecosystems, 10, 1069-1083.
doi: 10.1007/s10021-007-9080-5
[35] White RP, Murray S, Rohweder M ( 2000). Pilot Analysis of Global Ecosystems: Grassland Ecosystems. World Resources Institute, Washington DC.
[36] Wilsey BJ, Parent G, Roulet NT, Moore TR, Potvin C ( 2002). Tropical pasture carbon cycling: Relationships between C source/sink strength, above-ground biomass and grazing. Ecology Letters, 5, 367-376.
doi: 10.1046/j.1461-0248.2002.00322.x
[37] Wu GL, Liu ZH, Zhang L, Chen JM, Hu TM ( 2010). Long-term fencing improved soil properties and soil organic carbon storage in an alpine swamp meadow of western China. Plant and Soil, 332, 331-337.
doi: 10.1007/s11104-010-0299-0
[38] Xie XL, Sun B, Zhou HZ, Li ZP, Li AB ( 2004). Organic carbon density and storage in soils of China and spatial analysis. Acta Pedologica Sinica, 41, 35-43.
[ 解宪丽, 孙波, 周慧珍, 李忠佩, 李安波 ( 2004). 中国土壤有机碳密度和储量的估算与空间分布分析. 土壤学报, 41, 35-43.]
[39] Yang YH, Mohammat A, Feng JM, Zhou R, Fang JY ( 2007). Storage, patterns and environmental controls of soil organic carbon in China. Biogeochemistry, 84, 131-141.
doi: 10.1111/gcb.14132 pmid: 29573504
[40] Zheng D, Zhang QS, Wu SH ( 2000). Mountain Geoecology and Sustainable Development of the Tibetan Plateau. Springer, Dordrecht. 15-16.
[41] Zhou XM, Wang QJ, Zhao XQ ( 2001). Chinese Kobresia Meadows. Science Press, Beijing.
[ 周兴民, 王启基, 赵新全 ( 2001). 中国嵩草草甸. 科学出版社, 北京.]
[42] Zibilske LM ( 1994). Carbon mineralization. In Weaver RW, Angle S, Bottomley P, Bezdicek D, Smith S, Tabatabai A, Wollum A eds. Methods of Soil Analysis. Part 2—‌Microbiological and Biochemical Properties. Soil Science Society of America, Wisconsin, USA. 835-863.
doi: 10.1016/j.scitotenv.2019.135969 pmid: 31838422
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[1] Yang Ying-gen;Zhang Li-jun and Li yu. Studies on the Postharvest Physiology properties of Peach Fruits[J]. Chin Bull Bot, 1995, 12(04): 47 -49 .
[2] Zhou Shi-gong. Applications of Lanthanum in Botanical Research[J]. Chin Bull Bot, 1992, 9(02): 26 -29 .
[3] . [J]. Chin Bull Bot, 1996, 13(专辑): 105 .
[4] 杜维广 王彬如 谭克辉 郝迺斌. An Approach to the Breeding of Soybean with High Photosynthetic Efficiency[J]. Chin Bull Bot, 1984, 2(23): 7 -11 .
[5] ZHAO Yun-Yun ZHOU Xiao-Mei YANG Cai. Production of Hybrid F1 Between Avena magna and Avena nuda and It''s Identification[J]. Chin Bull Bot, 2003, 20(03): 302 -306 .
[6] . Professor Jiayang Li, a Plant Molecular Genetist[J]. Chin Bull Bot, 2003, 20(03): 370 -372 .
[7] . [J]. Chin Bull Bot, 1996, 13(专辑): 100 -101 .
[8] Qiong Jiang, Youning Wang, Lixiang Wang, Zhengxi Sun, Xia Li. Validation of Reference Genes for Quantitative RT-PCR Analysis in Soybean Root Tissue under Salt Stress[J]. Chin Bull Bot, 2015, 50(6): 754 -764 .
[9] MA Ke-Ming. Advances of the Study on Species Abundance Pattern[J]. Chin J Plan Ecolo, 2003, 27(3): 412 -426 .