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Variations in the foliar δ13C and C3/C4 species richness in the Japanese flora of Poaceae among climates and habitat types under human activity

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Ecological Research

Abstract

For 383 Poaceae species harvested over the Japanese islands and stored as herbarium specimens along several decades, we determined C3 and C4 types of photosynthesis from leaf stable carbon isotope ratio (δ13C). Then, we sought the relationships between C4 species richness and climatic factors or habitat types. Except for the two Panicum species (P. lanuginosum and P. scoparium) having the possibility of C3–C4 intermediate, 227 and 154 species were classified into C3 and C4. The C4 species richness increased from northern to southern islands in Japan, positively correlated with mean annual air temperature. Greater C4 species richness in the seashore habitats, and smaller C4 species richness in the shaded, wet and highland habitats would be related to the photosynthetic responses to local environmental factors such as irradiance level and temperature regime. No difference of leaf δ-value of C3 Poaceae was obtained between the habitats with different soil water availability, suggesting the less importance of soil water availability on leaf water-use efficiency in C3 Poaceae species in Japan having humid climate. Additionally, possible effects of human activity around the harvested time or site on leaf δ-value were estimated, because the habitat includes the sites with high human activity. Leaf δ-value was decreased with sampling year, and it was higher in the densely inhabited district for both C3 and C4. They are probably due to a historical decrease in the atmospheric δ-value via increasing human activity, and high gas emission at the districts of high human density.

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References

  • Aikawa M, Yoshikawa K, Tomida M, Aotsuka F, Haraguchi H (1995) Continuous monitoring of the carbon dioxide concentration in the urban atmosphere of Nagoya, 1991–1993. Anal Sci 11:357–362. doi:10.2116/analsci.11.357

    Article  CAS  Google Scholar 

  • Bender MM, Smith D (1973) Classification of starch- and fructosan-accumulating grasses as C-3 or C-4 species by carbon isotope analysis. J Br Grassland Soc 28:97–100. doi:10.1111/j.1365-2494.1973.tb00727.x

    Article  CAS  Google Scholar 

  • Broadmeadow MSJ, Griffiths H (1993) Carbon isotope discrimination and the coupling of CO2 fluxes within forest canopies. In: Ehleringer JR, Hall AE, Farquhar GD (eds) Stable isotopes and plant carbon–water relations. Academic Press, New York, pp 109–129

    Google Scholar 

  • Brown RH, Hattersley PW (1989) Leaf anatomy of C3–C4 species as related to evolution of C4 photosynthesis. Plant Physiol 91:1543–1550

    Article  PubMed  Google Scholar 

  • Brown RH, Bouton JH, Evans PT, Malter HE, Rigsby LL (1985) Photosynthesis, morphology, leaf anatomy, and cytogenetics of hybrids between C3 and C3/C4 Panicum species. Plant Physiol 77:653–658

    Article  PubMed  Google Scholar 

  • Buchmann N, Brooks J, Rapp K, Ehleringer J (1996) Carbon isotope composition of C4 grasses is influenced by light and water supply. Plant Cell Environ 19:392–402. doi:10.1111/j.1365-3040.1996.tb00331.x

    Article  CAS  Google Scholar 

  • Clayton WD, Renvoize S (1986) Genera graminum, grasses of the world. Kew Bull Addit Ser 13:1–389

    Google Scholar 

  • Crawley M, Harvey P, Purvis A (1997) Comparative ecology of the native and alien floras of the British Isles. In: Silvertown JW, Harper JL (eds) Plant life histories: ecology, phylogeny and evolution. Cambridge University Press, New York, pp 36–56

    Google Scholar 

  • Dongarrà G, Varrica D (2002) δ13C variations in tree rings as an indication of severe changes in the urban air quality. Atmos Environ 36:5887–5896. doi:10.1016/S1352-2310(02)00824-5

    Article  Google Scholar 

  • Ehleringer J, Buchmann N, Flanagan L (2000) Carbon isotope ratios in belowground carbon cycle processes. Ecol Appl 10:412–422

    Article  Google Scholar 

  • Farquhar GD, O’Leary MH, Berry JA (1982) On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Aust J Plant Physiol 9:121–137. doi:10.1071/PP9820121

    Article  CAS  Google Scholar 

  • Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 40:503–537. doi:10.1146/annurev.pp.40.060189.002443

    Article  CAS  Google Scholar 

  • Francey RJ, Gifford RM, Sharkey TD, Weir B (1985) Physiological influences on carbon isotope discrimination in Huon Pine (Lagarostrobos franklinii). Oecologia 66:211–218. doi:10.1007/BF00379857

    Google Scholar 

  • Francey RJ, Allison CE, Etheridge DM, Trudinger CM, Enting IG, Leuenberger M, Langenfelds RL, Michel E, Steele LP (1999) A 1000-year high precision record of δ13C in atmospheric CO2. Tellus B 51:170–193

    Article  Google Scholar 

  • Gamo T, Tsutsumi M, Sakai H, Nakazawa T, Machida T, Honda H, Itoh T (1995) Long-term monitoring of carbon and oxygen isotope ratios of stratospheric CO2 over Japan. Geophys Res Lett 22:397–400

    Article  CAS  Google Scholar 

  • Giussani LM, Nchez JHC-S, Zuloaga FO, Kellogg EA (2001) Molecular phylogeny of the grass subfamily Panicoideae (Poaceae) shows multiple origins of C4 photosynthesis. Am J Bot 88:1993–2012

    Article  CAS  Google Scholar 

  • Grass Phylogeny Working Group (2001) Phylogeny and subfamilial classification of the grasses (Poaceae). Ann Mo Bot Gard 88:373–457

    Article  Google Scholar 

  • Griffiths H (1992) Carbon isotope discrimination and the integration of carbon assimilation pathways in terrestrial CAM plants. Plant Cell Environ 15:1051–1062. doi:10.1111/j.1365-3040.1992.tb01655.x

    Article  CAS  Google Scholar 

  • Hanba YT, Mori S, Lei TT, Koike T, Wada E (1997) Variations in leaf δ13C along a vertical profile of irradiance in a temperate Japanese forest. Oecologia 110:253–261. doi:10.1007/s004420050158

    Article  Google Scholar 

  • Hanba YT, Noma N, Umeki K (2000) Relationship between leaf characteristics, tree sizes and species distribution along a slope in a warm temperate forest. Ecol Res 15:393–403. doi:10.1046/j.1440-1703.2000.00360.x

    Article  Google Scholar 

  • Hanba YT, Fujino M, Ushijima H, Kazama T, Kagotani Y (2009) Application of stable carbon isotopes on plant physiological processes and urban ecosystem. In: Okouchi N, Tayasu I, Koba K (eds) Earth, life, and isotopes. Kyoto University Press, Kyoto (in press)

  • Hattersley PW, Watson L (1992) Diversification of photosynthesis. In: Chapman GP (ed) Grass evolution and domestication. Cambridge University Press, London, pp 38–116

    Google Scholar 

  • Henderson S, von Caemmerer S, Farquhar GD (1992) Short-term measurements of carbon isotope discrimination in several C4 species. Aust J Plant Physiol 19:263–285. doi:10.1071/PP9920263

    Article  CAS  Google Scholar 

  • Holaday AS, Black CC (1981) Comparative characterization of phosphoenolpyruvate carboxylase in C3, C4, and C3–C4 intermediate Panicum species. Plant Physiol 67:330–334

    Article  CAS  PubMed  Google Scholar 

  • Kitamura S, Murata G, Koyama T (2004) Colored illustrations of herbaceous plants of Japan vol. III (Monocotyledoneae). Hoikusha Publishing Co., Ltd, Higashiosaka

    Google Scholar 

  • Kogami H, Hanba YT, Kibe T, Terashima I, Masuzawa T (2001) CO2 transfer conductance, leaf structure and carbon isotope discrimination of Polygonum cuspidatum leaves from low and high altitude. Plant Cell Environ 24:529–538. doi:10.1046/j.1365-3040.2001.00696.x

    Article  CAS  Google Scholar 

  • Körner C, Farquhar GD, Roksandic Z (1988) A global survey of carbon isotope discrimination in plants from high altitude. Oecologia 74:623–632. doi:10.1007/BF00328400

    Article  Google Scholar 

  • Körner C, Farquhar GD, Wong SC (1991) Carbon isotope discrimination by plants follows latitudinal and altitudinal trends. Oecologia 88:30–40. doi:10.1007/BF00380063

    Article  Google Scholar 

  • Kubásek J, Šetlík J, Dwyer S, Šantrůček J (2007) Light and growth temperature alter carbon isotope discrimination and estimated bundle sheath leakiness in C4 grasses and dicots. Photosyn Res 91:47–58. doi:10.1007/s11120-007-9136-6

    Article  PubMed  Google Scholar 

  • Kume A, Satomura T, Tsuboi N, Chiwa M, Hanba YT, Nakane K, Horikoshi T, Sakugawa H (2003) Effects of understory vegetation on the ecophysiological characteristics of an overstory pine, Pinus densiflora. For Ecol Manag 176:195–203. doi:10.1016/S0378-1127(02)00282-7

    Article  Google Scholar 

  • Lichtfouse E, Lichtfouse M, Jaffrézic A (2003) δ13C values of grasses as a novel indicator of pollution by fossil-fuel-derived greenhouse gas CO2 in urban areas. Environ Sci Technol 37:87–89

    Article  CAS  PubMed  Google Scholar 

  • Lloyd J, Farquhar GD (1994) 13C discrimination during CO2 assimilation by the terrestrial biosphere. Oecologia 99:201–215. doi:10.1007/BF00627732

    Article  Google Scholar 

  • Long SP (1999) Environmental responses. In: Sage RS, Monson RK (eds) C4 plant biology. Academic Press, New York, pp 215–249

    Chapter  Google Scholar 

  • Long S, Mason C (1983) Saltmarsh ecology. Glasgou, UK

    Google Scholar 

  • Mishio M, Kawakubo N (2000) Phenological differences and similarities between C3 and C4 grasses in sunny habitats with contrasting moisture levels. Jpn J Ecol 50:93–98

    Google Scholar 

  • Mo W, Nishimura N, Soga Y, Yamada K, Yoneyama T (2004) Distribution of C3 and C4 plants and changes in plant and soil carbon isotope ratios with altitude in the Kirigamine grassland, Japan. Grassland Sci 50:243–254

    CAS  Google Scholar 

  • Morita H (2002) Development of identification methods and elucidation of emergence ecology on gramineous weeds of paddy fields in Japan. J Weed Sci Technol 47:175–184

    Google Scholar 

  • Murphy BP, Bowman DMJS (2007) Seasonal water availability predicts the relative abundance of C3 and C4 grasses in Australia. Glob Ecol Biogeogr 16:160–169. doi:10.1111/j.1466-8238.2006.00285.x

    Article  Google Scholar 

  • National Astronomical Observatory (2008) Chronological scientific tables 2004. Maruzen Co., Ltd., Tokyo

    Google Scholar 

  • Nishimura N, Soga Y, Tsuda S, Saijoh Y, Mo W (1997) Altitudinal variation in the species composition of main grasses in the Kirigamine subalpine grassland. J Jpn Soc Grassland Sci 42:324–334

    Google Scholar 

  • O’Leary MH (1988) Carbon isotopes in photosynthesis. Bioscience 38:328–336

    Article  Google Scholar 

  • Oguro H, Hinata K, Tsunoda S (1985) Comparative anatomy and morphology of leaves between C3 and C4 species in Panicum. Ann Bot 55:859–867

    Google Scholar 

  • Okuda T (1987) The distribution of C3 and C4 graminoids on the semi-natural grassland of southwestern Japan. J Jpn Soc Grassland Sci 33:175–184

    Google Scholar 

  • Okuda T, Furukawa A (1990) Occurrence and distribution of C4 plants in Japan. Jpn J Ecol 40:91–121

    Google Scholar 

  • Osada T (1993) Illustrated grasses of Japan. Enlarged Edition. Heibonsha Ltd., Tokyo

    Google Scholar 

  • Paruelo JM, Lauenroth WK (1996) Relative abundance of plant functional types in grasslands and shrublands of North America. Ecol Appl 6:1212–1224

    Article  Google Scholar 

  • Paruelo JM, Jobbágy EG, Sala OE, Lauenroth WK, Burke IC (1998) Functional and structural convergence of temperate grassland and shrubland ecosystems. Ecol Appl 8:194–206

    Article  Google Scholar 

  • Pataki DE, Bush SE, Ehleringer JR (2007) Stable isotopes as a tool in urban ecology. In: Flanagan LB, Ehleringer JR, Pataki DE (eds) Stable isotopes and biosphere–atmosphere interactions: processes and biological controls. Elsevier Academic Press, Amsterdam, pp 199–214

    Google Scholar 

  • Pearcy RW (1990) Sunflecks and photosynthesis in plant canopies. Annu Rev Plant Physiol Plant Mol Biol 41:421–453. doi:10.1146/annurev.pp.41.060190.002225

    Article  CAS  Google Scholar 

  • Randerson JT (2007) Terrestrial ecosystems and interannual variability in the global atmospheric budgets of 13CO2 and 12CO2. In: Flanagan LB, Ehleringer JR, Pataki DE (eds) Stable isotopes and biosphere–atmosphere interactions: processes and biological controls. Elsevier Academic Press, Amsterdam, pp 217–234

    Google Scholar 

  • Sage RF, Kubien DS (2007) The temperature response of C3 and C4 photosynthesis. Plant Cell Environ 30:1086–1106. doi:10.1111/j.1365-3040.2007.01682.x

    Article  CAS  PubMed  Google Scholar 

  • Sage RF, Meirong L, Monson RK (1999a) The taxonomic distribution of C4 photosynthesis. In: Sage RF, Monson RK (eds) C4 plant biology. Academic Press, New York

    Google Scholar 

  • Sage RF, Wedin DA, Meirong L (1999b) The biogeography of C4 photosynthesis: patterns and controlling factors. In: Sage RF, Monson RK (eds) C4 plant biology. Academic Press, New York, pp 313–356

    Chapter  Google Scholar 

  • Saurer M, Siegwolf RTW, Schweingruber FH (2004) Carbon isotope discrimination indicates improving water-use efficiency of trees in northern Eurasia over the last 100 years. Glob Chang Biol 10:2109–2120. doi:10.1111/j.1365-2486.2004.00869.x

    Article  Google Scholar 

  • Shimizu N, Morita H, Hirota S (2002) Photographs of naturalized plants in Japan. Zenkoku Noson Kyoiku Kyokai, Tokyo

    Google Scholar 

  • Song M, Duan D, Chen H, Hu Q, Zhang F, Xu X, Tian Y, Ouyang H, Peng C (2008) Leaf δ13C reflects ecosystem patterns and responses of alpine plants to the environments on the Tibetan Plateau. Ecography 31:499–508. doi:10.1111/j.0906-7590.2008.05331.x

    Article  Google Scholar 

  • Suzuki S (1996) Illustration of Japanese Bambusaceae (revised edition). Jyukai Shorin, Funabashi

    Google Scholar 

  • Takeda T, Tanikawa T, Agata W, Hakoyama S (1985) Studies on the ecology and geographical distribution of C3 and C4 grasses. Jpn J Crop Sci 54:54–64

    Google Scholar 

  • Takematsu T, Ichizen N (1997) Weeds of the world volume III, monocotyledoneae. Zenkoku Noson Kyoiku Kyokai, Tokyo

    Google Scholar 

  • Tateoka A (1959) Explanation of Poaceae plants. Meibun-do, Tokyo

    Google Scholar 

  • Tazoe Y, Noguchi K, Terasima I (2006) Effects of growth light and nitrogen nutrition on the organization of the photosynthetic apparatus in leaves of a C4 plant, Amaranthus cruentus. Plant Cell Environ 29:691–700. doi:10.1111/j.1365-3040.2005.01453.x

    Article  CAS  PubMed  Google Scholar 

  • Ueno O, Takeda T (1992) Photosynthesis pathways, ecological characteristics, and the geographical distribution of the Cyperaceae in Japan. Oecologia 89:195–203. doi:10.1007/BF00317218

    Google Scholar 

  • Vogel JC (1993) Variability of carbon isotope fractionation during photosynthesis. In: Ehleringer JR, Hall AE, Farquhar GD (eds) Stable isotopes and plant carbon–water relations. Academic Press, New York, pp 29–46

    Google Scholar 

  • von Caemmerer S (1992) Carbon isotope discrimination in C3–C4 intermediates. Plant Cell Environ 15:1063–1072. doi:10.1111/j.1365-3040.1992.tb01656.x

    Article  Google Scholar 

  • von Caemmerer S, Furbank RT (1999) Modeling C4 photosynthesis. In: Sage RF, Monson RK (eds) C4 plant biology. Academic Press, New York, pp 173–211

    Chapter  Google Scholar 

  • von Caemmerer S, Hubick KT (1989) Short-term carbon-isotope discrimination in C3–C4 intermediate species. Planta 178:475–481. doi:10.1007/BF00963817

    Article  Google Scholar 

  • Waller SS, Lewis JK (1979) Occurrence of C3 and C4 photosynthetic pathways in North American grasses. J Range Manag 32:12–28

    Article  CAS  Google Scholar 

  • Wang RZ (2007) δ13C values, photosynthetic pathways, and plant functional types for some plants from saline meadow, northeastern China. Photosynthetica 45:18–22. doi:10.1007/s11099-007-0003-7

    Article  CAS  Google Scholar 

  • Wedin DA, Tilman D (1996) Influence of nitrogen loading and species composition on the carbon balance of grasslands. Science 274:1720–1723. doi:10.1126/science.274.5293.1720

    Article  CAS  PubMed  Google Scholar 

  • Widory D, Javoya M (2003) The carbon isotope composition of atmospheric CO2 in Paris. Earth Planet Sci Lett 215:289–298. doi:10.1016/S0012-821X(03)00397-2

    Article  CAS  Google Scholar 

  • Winter K, Holtum JAM (2002) How closely do the δ13C values of crassulacean acid metabolism plants reflect the proportion of CO2 fixed during day and night? Plant Physiol 129:1843–1851

    Article  CAS  PubMed  Google Scholar 

  • Yamashita M (2002) Naturalization of exotic pasture grasses. Grassland Sci 48:161–167

    Google Scholar 

  • Zimmerman JK, Ehleringer JR (1990) Carbon isotope ratios are correlated with irradiance levels in the Panamanian orchid Catasetum viridiflavum. Oecologia 83:247–249. doi:10.1007/BF00317759

    Article  Google Scholar 

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Acknowledgments

This work was supported by the JSPS Research Fellowship for Young Scientists (12740423-00) and Ohara Foundation at Research Institute for Bioresources, Okayama University (2004). Leaf δ-value was measured at the Center for Ecological Research, Kyoto University. We deeply appreciate Y. Kohata, H. Katayama, N. Kinosyita, T. Kose, Y. Kasahara, and the other 52 collaborators collecting Poaceae plant samples. We thank T. Yamamoto, N. Yoshida, and S. Senoo at Kyoto Institute of Technology and R. Kito and T. Ichikawa at Kagawa University for their help in checking data.

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Correspondence to Yuko T. Hanba.

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Hanba, Y.T., Kobayashi, T. & Enomoto, T. Variations in the foliar δ13C and C3/C4 species richness in the Japanese flora of Poaceae among climates and habitat types under human activity. Ecol Res 25, 213–224 (2010). https://doi.org/10.1007/s11284-009-0652-z

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