Abstract
To apply carbon isotope composition (δ 13C) analyses of C4 plants to the quantitative reconstruction of paleoclimate, the functional mechanism linking plant δ 13C (δ 13Cp) to the environment, which is based on the plants’ physiological characteristics and morphological adaptability, must be thoroughly understood. Foxtail millet (Setaria italic) and common millet (Panicum miliaceum), as C4 plants, are representative crops of the rain-fed agriculture present in northern China. Fossil millets are ideal for paleoclimatic studies because of the ease of acquisition and identification to the species level. Modern seeds of foxtail and common millet collected from different habitats of the Chinese Loess Plateau, and their carbon isotope compositions, were analyzed and correlated with environmental factors, such as latitude, altitude, temperature, precipitation, water availability, and relative humidity. The results showed that the δ 13C of foxtail millet had a significantly negative correlation with latitude (R=-0.46), which may indicate the influence of light. The effect of light on the δ 13C of foxtail millet accounted for only 21% of variability, while other climatic factors did not exert significant influences. Thus, the δ 13C of foxtail millet was not suitable for extracting climatic information. The δ 13C of common millet was significantly and positively correlated with precipitation during the growing period (R=0.75), explaining 56% of variability. The functional mechanisms analyzed, using the plants’ physiological characteristics and morphological adaptability, indicated that common millet can adapt to environmental changes because of stomatal sensitivity and some non-stomatal factors. Therefore, the δ 13C of common millet can record precipitation during growth and is a promising factor for paleoclimatic reconstruction.
Similar content being viewed by others
References
Akhani H, Trimborn P, Ziegler H. 1997. Photosynthetic pathways in Chenopodiaceae from Africa, Asia and Europe with their ecological, phytogeographical and taxonomical importance. Plant Syst Evol, 206: 187–221
An Z M. 1988. Prehistoric agriculture in China (in Chinese). Acta Archaeol Sin, 4: 369–381
Anderson W T, Bernasconi S M, McKenzie J A, Saurer M. 1998. Oxygen and carbon isotopic record of climatic variability in tree ring cellulose (Picea abies): An example from central Switzerland (1913–1995). J Geophys Res: Atmospheres (1984–2012), 103: 31625–31636
Araus J L, Buxó R. 1993. Changes in carbon isotope discrimination in grain cereals from the North-Western Mediterranean Basin during the past seven millennia. Aust J Plant Physiol, 20: 117–128
Blum A. 2009. Effective use of water (EUW) and not water-use efficiency (WUE) is the target of crop yield improvement under drought stress. Field Crops Res, 112: 119–123
Bowman W D, Hubick K T, von Caemmerer S, Farquhar G D. 1989. Short-term changes in leaf carbon isotope discrimination in salt- and water-stressed C4 grasses. Plant Physiol, 90: 162–166
Brueck H. 2008. Effects of nitrogen supply on water-use efficiency of higher plants. J Plant Nutr Soil Sci, 171: 210
Buchmann N, Brooks J R, Rapp K D, Ehleringer J R. 2006. Carbon isotope composition of C4 grasses is influenced by light and water supply. Plant Cell Environ, 19: 392–402
von Caemmerer S, Furbank R T. 1999. The modelling of C4 photosynthesis. In: Sage R F, Monson R K, eds. C4 Plant Biology. San Diego: Academic Press. 173–211
Carmo-Silva A E, Powers S J, Keys A J, Arraba C A, Maria C, Parry M A J. 2008. Photorespiration in C4 grasses remains slow under drought conditions. Plant Cell Environ, 31: 925–940
Cerling T E, Wang Y, Quade J. 1993. Expansion of C4 ecosystems as an indicator of global ecological change in the late Miocene. Nature, 361: 344–345
Cerling T E, Harris J M, MacFadden B J, Leakey M G, Quade J, Eisenmann V, Ehleringer J R. 1997. Global vegetation change through the Miocene/Pliocene boundary. Nature, 389: 153–158
Cerling T E, Ehleringer J R, Harris J M. 1998. Carbon dioxide starvation, the development of C4 ecosystems, and mammalian evolution. Philos Trans R Soc B-Biol Sci, 353: 159–171
Cernusak L A, Ubierna N, Winter K, Holtum J A, Marshall J D, Farquhar G D. 2013. Environmental and physiological determinants of carbon isotope discrimination in terrestrial plants. New Phytol, 200: 1–16
Chai Y. 1999. Broomcorn Millet (in Chinese). Beijing: Chinese Agriculture Press
Chen S P, Bai Y F, Zhang L X, Han X G. 2005. Comparing physiological responses of two dominant grass species to nitrogen addition in Xilin River Basin of China. Environ Exp Bot, 53: 65
Ciais P, Tans P P, Trolier M, White J W C, Francey R J. 1995. A large northern hemisphere terrestrial CO2 sink indicated by the 13C/12C ratio of atmospheric CO2. Science, 269: 1098–1120
Comstock J P, Ehleringer J R. 1992. Correlating genetic variation in carbon isotopic composition with complex climatic gradients. Proc Natl Acad Sci USA, 89: 7747–7751
Crawford G W. 2006. East Asian Plant Domestication. In: Stark M T, ed. Archaeol Asia. Oxford: Blackwell Publishing. 77–95
Dawson T E, Mambelli S, Plamboeck A H, Templer P H, Tu K P. 2002. Stable isotopes in plant ecology. Annu Rev Ecol Syst, 33: 507–559
DeLucia E H, Schlesinger W H, Billings W D. 1988. Water relations and the maintenance of Sierran conifers on hydrothermally altered rock. Ecology, 69: 303–311
Dengler N G, Nelson T. 1999. Leaf structure and development in C4 plants. In: Sage R F, Russell K M, eds. C4 Plant Biology. San Diego: Academy Press. 133–172
DeNiro M J, Hastorf C A. 1985. Alteration of 15N/14N and 13C/12C ratios of plant matter during the initial stages of diagenesis: Studies utilizing archaeological specimens from Peru. Geochim Cosmochim Acta, 49: 97–115
Diefendorf A F, Mueller K E, Wing S L, Koch P L, Freeman K H. 2010. Global patterns in leaf 13C discrimination and implications for studies of past and future climate. Proc Natl Acad Sci USA, 107: 5738–5743
Drake B G, Gonzàlez-Meler M A, Long S P. 1997. More efficient plants: A Consequence of Rising Atmospheric CO2? Annu Rev Plant Phys, 48: 609–639
Ehleringer J R, Mooney H A. 1983. Photosynthesis and productivity of desert and Mediterranean climate plants. Encycloped Plant Physiol, 12: 205–231
Farquhar G D, Sharkey T D. 1982. Stomatal conductance and photosynthesis. Annu Rev Plant Phys, 33: 317–345
Farquhar G D. 1983. On the nature of carbon isotope discrimination in C4 species. Aust J Plant Physiol, 10: 205–226
Farquhar G D, Richards R A. 1984. Isotopic composition of plant carbon correlates with water-use efficiency of wheat genotypes. Aust J Plant Physiol, 11: 539–552
Farquhar G D, Ehleringer J R, Hubick K T. 1989. Carbon isotope discrimination and photosynthesis. Annu Rev Plant Phys, 40: 503–537
Francey R J, Farquhar G D. 1982. An explanation of 13C/12C variations in tree rings. Nature, 297: 28–31
Ghannoum O, von Caemmerer S, Conroy J P. 2002. The effect of drought on plant water use efficiency of 9 NAD-ME and NADP-ME C4 grasses. Funct Plant Biol, 29: 1337–1348
Ghannoum O, Conroy J P, Driscoll S P, Paul M J, Foyer C H, Lawlor D W. 2003. Non-stomatal limitations are responsible for drought-induced photosynthetic inhibition in four C4 grasses. New Phytol, 159: 835–844
Ghannoum O. 2009. C4 photosynthesis and water stress. Ann Bot, 103: 635–644
Goodfriend G A. 1990. Rainfall in the Negev desert during the middle Holocene, based on 13C of organic matter in land snail shells. Quat Res, 34: 186–197
Gouveia A C, Freitas H. 2009. Modulation of leaf attributes and water use efficiency in Quercus suber along a rainfall gradient. Trees, 23: 267–275
Gu S L, Ma J P, Liu Z J, Du J E, Guo Z L. 2001. Study on water use and water-saving techniques in foxtail millet (in Chinese with English abstract). Agr Res Arid Area, 19: 40–47
Gu Z Y, Liu Q, Xu B, Han J M, Yang S L, Ding Z L, Liu D S. 2003. Climate as the dominant control on C3 and C4 plant abundance in the Loess Plateau: Organic carbon isotope evidence from the last glacial-interglacial loess-soil sequences. Chin Sci Bull, 48: 1271–1276
Guehl J M, Fort C, Ferhi A. 1995. Differential response of leaf conductance, carbon isotope discrimination and water-use efficiency to nitrogen deficiency in maritime pine and pedunculate oak plants. New Phytol, 131: 149–157
Guo G, Xie G. 2006. The relationship between plant stable carbon isotope composition, precipitation and satellite data, Tibet Plateau, China. Quat Int, 144: 68–71
Hadley N F, Szarek S R. 1981. Productivity of desert ecosystems. Bioscience, 31: 747–753
Hatch M D. 1987. C4 photosynthesis: A unique blend of modified biochemistry, anatomy and ultrastructure. Biochim Biophys Acta, 895: 81–106
Hatch M D. 1999. C4 photosynthesis: A historical overview. In: Sage R F, Russell K M, eds. C4 Plant Biology. San Diego: Academy Press. 17–46
Hattersley P W. 1982. δ 13C values of C4 types in grasses. Aust J Plant Physiol, 9: 139–154
Hattersley P W. 1983. The distribution of C3 and C4 grasses in Australia in relation to climate. Oecologia, 57: 113–128
Hattersley P W, Watson L. 1992. Diversification of photosynthesis. In: Chapman G P, ed. Grass Evolution and Domestication. London: Cambridge University Press. 38–116
Hatté C, Antoine P, Fontugne M, Lang A, Rousseau D D, Zoller L. 2001. δ 13C of loess organic matter as a potential proxy for paleoprecipitation. Quat Res, 55: 33–38
Henderson S A, von Caemmerer S, Farquhar G D. 1992. Short-term measurements of carbon isotope discrimination in several C4 species. Aust J Plant Physiol, 19: 263–285
Hubick K T, Farquhar G D. 1987. Carbon isotope discrimination-selecting for water-use efficiency. Aust Cotton Grower, 8: 66–68
Hubick K T, Hammer G L, Farquhar G D, Wade L J, von Caemmerer S, Henderson S A. 1990. Carbon isotope discrimination varies genetically in C4 species. Plant Physiol, 92: 534–537
IPCC. 2007. Technical Summary. In: Solomon S, Qin D, Manning M, Alley R B, Berntsen T, Bindoff N L, Chen Z, Chidthaisong A, Gregory J M, Hegerl G C, Heimann M, Hewitson B, Hoskins B J, Joos F, Jouzel J, Kattsov V, Lohmann U, Matsuno T, Molina M, Nicholls N, Overpeck J, Raga G, Ramaswamy V, Ren J, Rusticucci M, Somerville R, Stocker T F, Whetton P, Wood R A, Wratt D, eds. Climate change 2007 The physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge: Cambridge University Press
Kalapos T, van den Boogaard R, Lambers H. 1996. Effect of soil drying on growth, biomass allocation and leaf gas exchange of two annual grass species. Plant Soil, 185: 137–149
Kohn M J. 2010. Carbon isotope compositions of terrestrial C3 plants as indicators of (paleo)ecology and (paleo)climate. Proc Natl Acad Sci USA, 107: 19691–19695
Körner C H, Diemer M. 1987. In situ Photosynthetic responses to light, temperature and carbon dioxide in herbaceous plants from low and high altitude. Funct Ecol, 1: 179–194
Körner C H, Larcher W. 1988. Plant life in cold climates. In: Long S P, Woodward F I, eds. Plants and Temperature. Sym Soc Exp Biol, 42: 25–57
Körner C, Farquhar G D, Roksandic Z. 1988. A global survey of carbon isotope discrimination in plants from high altitude. Oecologia, 74: 623–632
Körner C, Newmayer M, Menendez-Reidl S P, Smeets Scheel A. 1989. Functional morphology of mountain plants. Flora, 182: 353–383
Korol R L, Kirschbaum M U F, Farquhar G D, Jeffreys M. 1999. Effects of water status and soil fertility on the C-isotope signature in Pinus radiate. Tree Physiol, 19: 551–562
Leffler A J, Enquist B J. 2002. Carbon isotope composition of tree leaves from Guanacaste, Costa Rica: Comparison across tropical forests and tree life history. J Trop Ecol, 18: 151–159
Li J Z, Wang G A, Liu X Z, Han J M. 2009. Variations in carbon isotope ratios of C3 plants and distribution of C4 plants along an altitudinal transect on the eastern slope of Mount Gongga. Sci China Ser D-Earth Sci, 52: 1714–1723
Li X Q. 2013. New progress in the Holocene climate and agriculture research in China. Sci China Earth Sci, 56: 2027–2036
Liang Z S, Kang S Z. 1996. Water use efficiency and improvement way (in Chinese with English abstract). Acta Bot Boreal-Occidental Sin, 16: 79–84
Lin N F, Chai Y, Liao Q. 2002. Minor Grain Crops in China (in Chinese). Beijing: China Agriculture
Liu C J, Kong Z C. 2004. Morphological comparison of foxtail millet and broomcorn millet and its significance in archaeological identification (in Chinese with English abstract). Archaeol, 8: 76–83
Liu W G, Ning Y F, An Z S, Lu H Y, Cao Y N, Wu Z H. 2002. Carbon isotopic composition of modern soil and paleosol as a response to vegetation change on the Chinese Loess Plateau. Sci China Ser D-Earth Sci, 48: 93–99
Liu W G, Ning Y F, An Z S, Wu Z H, Lu H Y, Cao Y N. 2005. Carbon isotopic composition of modern soil and paleosol as a response to vegetation change on the Chinese Loess Plateau. Sci China Ser D-Earth Sci, 48: 93–99
Liu W G, Feng X H, Ning Y F, Zhang Q L, Cao Y N, An Z S. 2005. δ 13C variation of C3 and C4 plants across an Asian monsoon rainfall gradient in arid northwestern China. Glob Change Biol, 11: 1094–1100
Livingston N J, Guy R D, Sun Z J, Ethier G J. 1999. The effects of nitrogen stress on the stable carbon isotope composition, productivity and water use efficiency of white spruce (Picea glauca (Moench) Voss) seedlings. Plant Cell Environ, 22: 281
Lu T L D. 1998. Some botanical characteristics of green foxtail (Setaria viridis) and harvesting experiments on the grass. Antiquity, 72: 902–907
Lu H Y, Zhang J P, Liu K B, Wu N Q, Li Y M, Zhou K S, Ye M L, Zhang T Y, Zhang H J, Yang X Y, Shen L C, Xu D K, Li Q. 2009. Earliest domestication of common millet (Panicum miliaceum) in East Asia extended to 1000 years ago. Proc Natl Acad Sci USA, 18: 7367–7372
Ma J Y, Sun W, Liu X N, Chen F H. 2012. Variation in the stable carbon and nitrogen isotope composition of plants and soil along a precipitation gradient in northern China. PLoS One, 7: e51894
Macfarlane C, Adams M A, White D A. 2004. Productivity, carbon isotope discrimination and leaf traits of trees of Eucalyptus globulus Labill in relation to water availability. Plant Cell Environ, 27: 1515–1524
Marino B D, McElroy M B, Salawitch R J, Spaulding W G. 1992. Glacial- to-interglacial variations in the carbon isotopic composition of atmospheric CO2. Nature, 357: 461–466
Maroco J P, Pereira J S, Chaves M M. 2000. Growth, photosynthesis and water-use efficiency of two C4 Sahelian grasses subjected to water deficits. J Arid Environ, 45: 119–137
McCarroll D, Loader N J. 2004. Stable isotopes in tree rings. Quat Sci Rev, 23: 771–801
Mitchell A K, Hinckley T M. 1993. Effects of nitrogen concentration on photosynthesis and water use efficiency in Douglas-fir. Tree Physiol, 12: 403–410
Miller J M, Williams R J, Farquhar G D. 2001. Carbon isotope discrimination by a sequence of Eucalyptus species along a subcontinental rainfall gradient in Australia. Funct Ecol, 15: 222–232
Morecroft M D, Woodward F I. 1996. Experiments on the causes of altitudinal differences in the leaf nutrient contents, size and δ 13C of Alchemilla alpine. New Phytol, 134: 471–479
Murphy B P, Bowman D M J S. 2009. The carbon and nitrogen isotope composition of Australian grasses in relation to climate. Funct Ecol, 23: 1040–1049
Ning Y F, Liu W G, An Z S. 2008. A 130-ka reconstruction of precipitation on the Chinese Loess Plateau from organic carbon isotopes. Paleogeogr Paleoclimatol Paleoecol, 270: 59–63
Orchard K A, Cernusak L A, Hutley L B. 2010. Photosynthesis and wateruse efficiency of seedlings from northern Australian monsoon forest, savanna, and swamp habitats grown in a common garden. Funct Plant Biol, 37: 1050–1060
Pyankov V I, Gunin P D, Tsoog S, Black C C. 2000. C4 plants in the vegetation of Mongolia: Their natural occurrence and geographical distribution in relation to climate. Oecologia, 123: 15–31
Roden J S, Bowling D R, McDowell N G, Bond B J, Ehleringer J R. 2005. Carbon and oxygen isotope ratios of tree ring cellulose along a precipitation transect in Oregon, United States. J Geophys Res, 110: G02003, dio: 10.1029/2005JG000033
Saliendra N Z, Meinzer F C, Perry M, Thom M. 1996. Association between partitioning of carboxylase activity and bundle sheath leakiness to CO2, carbon isotope discrimination, photosynthesis, and growth in sugarcane. J Exp Bot, 47: 907–914
Schulze E D, Ellis R, Schulze W, Trimborn P, Ziegler H. 1996. Diversity, metabolic types and δ 13C carbon isotope ratios in the grass flora of Namibia in relation to growth form, precipitation and habitat conditions. Oecologia, 106: 352–369
Schulze E D, Williams R J, Farquhar G D, Schulze W, Langridge J, Miller J M, Walker B H. 1998. Carbon and nitrogen isotope discrimination and nitrogen nutrition of trees along a rainfall gradient in northern Australia. Aust J Plant Physiol, 25: 413–425
Sheriff D W, Nambiar E K S. 1991. Nitrogen Nutrition, Growth and Gas Exchange in Eucalyptus globulus Labill, SEEDLING. Aust J Plant Physiol, 18: 37–52
Smith S D, Osmond C B. 1987. Stem photosynthesis in a desert ephemeral, Eriogonum inflatum. Oecologia, 72: 533–541
Smith S D, Nowak R S. 1990. Ecophysiology of plants in the intermountain lowlands. In: Osmond C B, Pitelka L F, Hidy G M, eds. Plant Biology of the Basin and Range (Ecological Studies vol. 80). Berlin: Springer-Verlag. 179–241
Song M, Duan D Y, Chen H, Hu Q W, Zhang F, Xu X L, Tian Y Q, Hua O Y, Peng C H. 2008. Leaf δ 13C reflects ecosystem patterns and responses of alpine plants to the environments on the Tibetan Plateau. Ecography, 31: 499–508
Still C J, Berry J A, Collatz G J, DeFries R S. 2003. Global distribution of C3 and C4 vegetation: Carbon cycle implications. Glob Biogeochem Cycl, 17: 1–14
Swap R J, Aranibar J N, Dowty P R, Gilhooly W P, Macko S A. 2004. Natural abundance of 13C and 15N in C3 and C4 vegetation of southern Africa: Patterns and implications. Glob Change Biol, 10: 350–358
Tang Z C. 1983. On the study of drought ecophysiology in plants (in Chinese with English abstract). Acta Ecol Sinica, 3: 196–204
Tieszen L L, Hein D, Qvortrup S A, Troughton J H, Imbamba S K. 1979. Use of δ 13C values to determine vegetation selectivity in East African herbivores. Oecologia, 37: 351–359
Thornthwaite C W. 1948. An approach toward a rational classification of climate. Geogr Rev, 38: 55–94
Ubierna N, Sun W, Cousins A B. 2011. The efficiency of C4 photosynthesis under low light conditions: Assumptions and calculations with CO2 isotope discrimination. J Exp Bot, 62: 3119–3134
Valentini R, Matteucci G, Dolman A J, Schulze E-D, Rebmann C, Moors E J, Granier A, Gross P, Jensen N O, Pilegaard K, Lindroth A, Grelle A, Bernhofer C, Grünwald T, Aubinet M, Ceulemans R, Kowalski A S, Vesala T, Rannik Ü, Berbigier P, Loustau D, Guðmundsson J, Thorgeirsson H, Ibrom A, Morgenstern K, Clement R, Moncrieff J, Montagnani L, Minerbi S, Jarvis P G. 2000. Respiration as the main determinant of carbon balance in European forests. Nature, 404: 861–865
Wang G A, Han J M, Liu D S. 2003. The carbon isotope composition of C3 herbaceous plants in loess area of northern China. Sci China Ser D-Earth Sci, 46: 1069–1076
Wang G A, Han J M, Zhou L P, Xiong X G, Wu Z H. 2005. Carbon isotope ratios of plants and occurrences of C4 species under different soil moisture regimes in arid region of Northwest China. Physiol Plant, 125: 74–81
Wang G A, Han J M, Zhou L P, Xiong X G, Tan M, Wu Z H, Peng J. 2006. Carbon isotope ratios of C4 plants in loess areas of North China. Sci China Ser D-Earth Sci, 49: 97–102
Wang G A, Li J Z, Liu X Z, Li X Y. 2013b. Variation in carbon isotope ratios of plants across a temperature gradient along the 400 mm isoline of mean annual precipitation in north China and their relevance to paleovegetation reconstruction. Quat Sci Rev, 63: 83–90
Wang Y, Xu Y F, Khawaja S, Passey B H, Zhang C F, Wang X M, Li Q, Tseng Z J, Takeuchi G T, Deng T, Xie G P. 2013a. Diet and environment of a mid-Pliocene fauna from southwestern Himalaya: Paleo-elevation implications. Earth Planet Sci Lett, 376: 43–53
Williams D G, Gemplo V, Fravolini A, Leavitt S W, Wall G W, Kimball B A, Pinter P J, LaMorte R, Ottman M. 2001. Carbon isotope discrimination by sorghum bicolor under CO2 enrichment and drought. New Phytol, 150: 285–293
West J B, Bowen G J, Cerling T E, Ehleringer J R. 2006. Stable isotopes as one of nature’s ecological recorders. Trends Ecol Evol, 21: 408–414
Yang Q, Li X Q, Liu W G, Zhou X Y, Zhao K L, Sun N. 2011. Carbon isotope fractionation during low temperature carbonization of foxtail and common millets. Org Geochem, 42: 713–719
Yao F Y, Wang G A, Liu X J, Song L. 2011. Assessment of effects of the rising atmospheric nitrogen deposition on nitrogen uptake and longterm water-use efficiency of plants using nitrogen and carbon stable isotopes. Rapid Commum Mass Sp, 25: 1827–1836
Yao X Y, Deng Z Y, Pu J Y, Yao X H, Ma X X, Zhu G Q, Guo J Y. 2004. A study on ecoclimate of prosomillet and its suitable planting regions in Gansu (in Chinese with English abstract). Arid Meteorol, 22: 52–56
You X L. 1993. The question for origin and spread in both Foxtail millet and Common millet. Agr Hist China, 12: 1–13
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Yang, Q., Li, X. Investigation of the controlled factors influencing carbon isotope composition of foxtail and common millet on the Chinese Loess Plateau. Sci. China Earth Sci. 58, 2296–2308 (2015). https://doi.org/10.1007/s11430-015-5181-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11430-015-5181-8