The Rangeland Journal The Rangeland Journal Society
Rangeland ecology and management
RESEARCH ARTICLE (Open Access)

Grazing primarily drives the relative abundance change of C4 plants in the typical steppe grasslands across households at a regional scale

Qing Zhang A C D , Yong Ding B D , Wenjing Ma A , Sarula Kang A , Xin Li C , Jianming Niu A C E , Xiangyang Hou B E , Xiliang Li B and Sarula B
+ Author Affiliations
- Author Affiliations

A School of Life Sciences, Inner Mongolia University, Hohhot, 010021, China.

B Institute of Grassland Research, Chinese Academy of Agricultural Sciences, Hohhot, 010010, China.

C Sino-US Centre for Conservation, Energy and Sustainability Science in Inner Mongolia University, Hohhot, 010021, China.

D The authors have contributed equally to the paper.

E Corresponding authors. Emails: jmniu2005@163.com; houxy16@126.com

The Rangeland Journal 36(6) 565-572 https://doi.org/10.1071/RJ13050
Submitted: 15 May 2013  Accepted: 19 July 2014   Published: 14 August 2014

Abstract

Increases in temperature and grazing intensity are believed to promote the relative abundance of C4 plants in grassland communities in Inner Mongolia. However, there is a lack of understanding as to which factor is the primary driver at the household scale. The relative abundance of C4 plants in grassland communities within 32 households was monitored over a 5-year period (2008–12) in the typical steppe region of Inner Mongolia. The relationships between the mean annual temperature, grazing intensity and their combinations on the patterns of the relative abundance of C4 plants across the land managed by these households were analysed. The results showed that (1) the herbage mass of the typical steppe grassland was mainly composed of C3 plants (87%); (2) the C4 plants were more sensitive to, and can be used as indicators of, environmental changes. These C4 species included Cleistogenes squarrosa (Trin.) Keng, Chenopodium glaucum Linn. and Salsola collina Pall.; (3) both increasing temperature and grazing intensity promoted the relative abundance of C4 plants. Grazing intensity was the primary driver of the change in relative abundance of C4 plants in this region. Not only did grazing change the micro-environment of the grasslands, but also the C3 species were preferentially grazed by the livestock. Comparison of the results with previous studies on the temporal variation in the abundance of C4 plants suggests that the relative importance of grazing and climatic factors depends on the spatial scales of the studies, with climate being of greater importance at the regional rather than the household scale.

Additional keywords: grazing intensity, grazing preferences, Inner Mongolian grassland, temperature.


References

Altesor, A., Piñeiro, G., Lezama, F., Jackson, R., Sarasola, M., and Paruelo, J. (2006). Ecosystem changes associated with grazing in sub-humid South American grasslands. Journal of Vegetation Science 17, 323–332.
Ecosystem changes associated with grazing in sub-humid South American grasslands.CrossRef |

An, B., and Han, G. D. (2011). Effect of grazing intensity on underground biomass and carbon density in meadow steppe. Inner Mongolia Prataculture 23, 42–45.

Archibold, O. W. (1995). ‘Ecology of World Vegetation.’ (Chapman & Hall: London, UK.)

Auerswald, K., Wittmer, M., Bai, Y. F., Yang, H., Taube, F., Susenbeth, A., and Schnyder, H. (2012). C4 abundance in an Inner Mongolia grassland system is driven by temperature-moisture interaction, not grazing pressure. Basic and Applied Ecology 13, 67–75.
C4 abundance in an Inner Mongolia grassland system is driven by temperature-moisture interaction, not grazing pressure.CrossRef |

Bell, M. J., Eckard, R. J., and Cullen, B. R. (2012). The effect of future climate scenarios on the balance between productivity and greenhouse gas emissions from sheep-grazing systems. Livestock Science 147, 126–138.
The effect of future climate scenarios on the balance between productivity and greenhouse gas emissions from sheep-grazing systems.CrossRef |

Borcard, D., Legendre, P., and Drapeau, P. (1992). Partialling out the spatial component of ecological variation. Ecology 73, 1045–1055.
Partialling out the spatial component of ecological variation.CrossRef |

Braak, C., and Smilauer, P. (2002). CANOCO Reference Manual and User’s Guide to Canoco for Windows: Software for Canonical Community Ordination (Version 4.5).’ (Microcomputer Power: Ithaca, New York.)

Casal, J. J., Sachz, R. A., and Deregibus, V. A. (1987). Tillering responses of Lolium multiflorum plants to changes of red/far-red ratio typical of sparse canopies. Journal of Experimental Botany 38, 1432–1439.
Tillering responses of Lolium multiflorum plants to changes of red/far-red ratio typical of sparse canopies.CrossRef |

Cerling, T. E., Wang, Y., and Quade, J. (1993). Expansion of C4 ecosystems as an indicator of global ecological change in the late Miocene. Nature 361, 344–345.
Expansion of C4 ecosystems as an indicator of global ecological change in the late Miocene.CrossRef |

Collins, S. L., and Calabrese, L. B. (2012). Effects of fire, grazing and topographic variation on vegetation structure in tallgrass prairie. Journal of Vegetation Science 23, 563–575.
Effects of fire, grazing and topographic variation on vegetation structure in tallgrass prairie.CrossRef |

Crush, J., and Rowarth, J. (2007). The role of C4 grasses in New Zealand pastoral systems. New Zealand Journal of Agricultural Research 50, 125–137.
The role of C4 grasses in New Zealand pastoral systems.CrossRef |

Deregibus, V. A., Sanchez, R. A., Casal, J. J., and Trlica, M. J. (1985). Tillering responses to enrichment of red light beneath the canopy in a humid natural grassland. Journal of Applied Ecology 22, 199–206.
Tillering responses to enrichment of red light beneath the canopy in a humid natural grassland.CrossRef |

Derner, J. D., Boutton, T. W., and Briske, D. D. (2006). Grazing and ecosystem carbon storage in the North American Great Plains. Plant and Soil 280, 77–90.
Grazing and ecosystem carbon storage in the North American Great Plains.CrossRef | 1:CAS:528:DC%2BD28XhslOrs7w%3D&md5=8c379ba6bcab961ddc7cd238ac87c922CAS |

Fanselow, N., Schoenbach, P., Gong, X. Y., Lin, S., Taube, F., Loges, R., Pan, Q., and Dittert, K. (2011). Short-term regrowth responses of four steppe grassland species to grazing intensity, water and nitrogen in Inner Mongolia. Plant and Soil 340, 279–289.
Short-term regrowth responses of four steppe grassland species to grazing intensity, water and nitrogen in Inner Mongolia.CrossRef | 1:CAS:528:DC%2BC3MXitFGkt7w%3D&md5=4c50f27791d5c3c10ccd8e6b29b4621dCAS |

Farquhar, G. D., Ehleringer, J. R., and Hubick, K. T. (1989). Carbon isotope discrimination and photosynthesis. Annual Review of Plant Biology 40, 503–537.
Carbon isotope discrimination and photosynthesis.CrossRef | 1:CAS:528:DyaL1MXktlKmu70%3D&md5=12b6e7eb49ee78f994a152e286b19830CAS |

Franz-Odendaal, T. A., Lee-Thorp, J. A., and Chinsamy, A. (2002). New evidence for the lack of C4 grassland expansions during the early Pliocene at Langebaanweg, South Africa. Paleobiology 28, 378–388.
New evidence for the lack of C4 grassland expansions during the early Pliocene at Langebaanweg, South Africa.CrossRef |

Hou, X.-Y., Han, Y., and Li, Y. (2012). The perception and adaptation of herdsmen to climate change and climate variability in the desert steppe region of northern China. The Rangeland Journal 34, 349–357.
The perception and adaptation of herdsmen to climate change and climate variability in the desert steppe region of northern China.CrossRef |

Jolly, D., and Haxeltine, A. (1997). Effect of low glacial atmospheric CO2 on tropical African montane vegetation. Science 276, 786–788.
Effect of low glacial atmospheric CO2 on tropical African montane vegetation.CrossRef | 1:CAS:528:DyaK2sXivFOrsro%3D&md5=fea91663cf82dc96cbfdcce3b6056bc6CAS | 9115201PubMed |

Kang, X., Hao, Y., Li, C., Cui, X., Wang, J., Rui, Y., Niu, H., and Wang, Y. (2011). Modeling impacts of climate change on carbon dynamics in a steppe ecosystem in Inner Mongolia, China. Journal of Soils and Sediments 11, 562–576.
Modeling impacts of climate change on carbon dynamics in a steppe ecosystem in Inner Mongolia, China.CrossRef | 1:CAS:528:DC%2BC3MXmtVCqsLo%3D&md5=9795b530fd1e4ba3c0dfcd6f90fb70fdCAS |

Kohn, M. J. (2010). Carbon isotope compositions of terrestrial C3 plants as indicators of (paleo)ecology and (paleo)climate. Proceedings of the National Academy of Sciences of the United States of America 107, 19 691–19 695.
Carbon isotope compositions of terrestrial C3 plants as indicators of (paleo)ecology and (paleo)climate.CrossRef | 1:CAS:528:DC%2BC3cXhsVymu7bI&md5=495d2860e7b7b5a34e65b28523e9c1b8CAS |

Leegood, R. C. (2013). Strategies for engineering C4 photosynthesis. Journal of Plant Physiology 170, 378–388.
Strategies for engineering C4 photosynthesis.CrossRef | 1:CAS:528:DC%2BC38XhvVekt7bL&md5=fb5ec2ef8e7ce4a715c4df01e78f1505CAS | 23245935PubMed |

Li, Y. P., and Ji, J. J. (2004). Assessment of the productivity and livestock carrying capacity of Inner Mongolia grassland by regional scale modeling. Journal of Natural Resources 19, 610–616.

Li, S. G., Harazono, Y., Oikawa, T., Zhao, H. L., He, Z. Y., and Chang, X. L. (2000). Grassland desertification by grazing and the resulting micrometeorological changes in Inner Mongolia. Agricultural and Forest Meteorology 102, 125–137.
Grassland desertification by grazing and the resulting micrometeorological changes in Inner Mongolia.CrossRef |

Li, W. J., Ali, S. H., and Zhang, Q. (2007). Property rights and grassland degradation: a study of the Xilingol Pasture, Inner Mongolia, China. Journal of Environmental Management 85, 461–470.
Property rights and grassland degradation: a study of the Xilingol Pasture, Inner Mongolia, China.CrossRef |

Liang, C., Michalk, D., and Millar, G. (2002). The ecology and growth patterns of Cleistogenes species in degraded grasslands of eastern Inner Mongolia, China. Journal of Applied Ecology 39, 584–594.
The ecology and growth patterns of Cleistogenes species in degraded grasslands of eastern Inner Mongolia, China.CrossRef |

Mavromihalis, J. A., Dorrough, J., Clark, S. G., Turner, V., and Moxham, C. (2013). Manipulating livestock grazing to enhance native plant diversity and cover in native grasslands. The Rangeland Journal 35, 95–108.
Manipulating livestock grazing to enhance native plant diversity and cover in native grasslands.CrossRef |

McPherson, G. R., and Rasmussen, G. A. (1989). Seasonal herbivory effects on herbaceous plant communities of the Edwards plateau Texas, USA. The Texas Journal of Science 41, 59–70.

McWilliam, J. R. (1978). Response of pasture plants to temperature. In: ‘Plant Relations in Pastures’. (Ed. J. R. Wilson.) pp. 17–34. (CSIRO Publishing: Melbourne.)

Norman, H. C., Wilmot, M. G., Thomas, D. T., Masters, D. G., and Revell, D. K. (2009). Stable carbon isotopes accurately predict diet selection by sheep fed mixtures of C3 annual pastures and saltbush or C4 perennial grasses. Livestock Science 121, 162–172.
Stable carbon isotopes accurately predict diet selection by sheep fed mixtures of C3 annual pastures and saltbush or C4 perennial grasses.CrossRef |

Owensby, C. E., Ham, J., Knapp, A., and Auen, L. (1999). Biomass production and species composition change in a tallgrass prairie ecosystem after long-term exposure to elevated atmospheric CO2. Global Change Biology 5, 497–506.
Biomass production and species composition change in a tallgrass prairie ecosystem after long-term exposure to elevated atmospheric CO2.CrossRef |

Pushkina, D., Bocherens, H., Chaimanee, Y., and Jaeger, J. J. (2010). Stable carbon isotope reconstructions of diet and paleoenvironment from the late Middle Pleistocene Snake Cave in North-eastern Thailand. Naturwissenschaften 97, 299–309.
Stable carbon isotope reconstructions of diet and paleoenvironment from the late Middle Pleistocene Snake Cave in North-eastern Thailand.CrossRef | 1:CAS:528:DC%2BC3cXhslehtrk%3D&md5=e7e3f820e8efa1de143d93f945bcd0baCAS | 20127068PubMed |

Reeder, J. D., Schuman, G. E., Morgan, J. A., and Lecain, D. R. (2004). Response of organic and inorganic carbon and nitrogen to long-term grazing of the shortgrass steppe. Environmental Management 33, 485–495.
Response of organic and inorganic carbon and nitrogen to long-term grazing of the shortgrass steppe.CrossRef | 15453402PubMed |

Ren, H., Schönbach, P., Wan, H., Gierus, M., and Taube, F. (2012). Effects of grazing intensity and environmental factors on species composition and diversity in typical steppe of Inner Mongolia, China. PLoS ONE 7, e52180.
Effects of grazing intensity and environmental factors on species composition and diversity in typical steppe of Inner Mongolia, China.CrossRef | 1:CAS:528:DC%2BC3sXlsVOjtA%3D%3D&md5=20bfa2b3454892421d3bc6595873b440CAS | 23284925PubMed |

Ripley, B. S., Cunniff, J., and Osborne, C. P. (2013). Photosynthetic acclimation and resource use by the C3 and C4 subspecies of Alloteropsis semialata in low CO2 atmospheres. Global Change Biology 19, 900–910.
Photosynthetic acclimation and resource use by the C3 and C4 subspecies of Alloteropsis semialata in low CO2 atmospheres.CrossRef | 23504846PubMed |

Sage, R. F. (2004). The evolution of C4 photosynthesis. New Phytologist 161, 341–370.
The evolution of C4 photosynthesis.CrossRef | 1:CAS:528:DC%2BD2cXhsVymuro%3D&md5=b1c61a8f612aa6f633fac0b3cfa15287CAS |

Sage, R. F., and Kubien, D. S. (2007). The temperature response of C3 and C4 photosynthesis. Plant, Cell & Environment 30, 1086–1106.
The temperature response of C3 and C4 photosynthesis.CrossRef | 1:CAS:528:DC%2BD2sXhtVeiurrP&md5=75b7c196aa464b647364fb5ce4224605CAS |

Sage, R. F., Wedin, D. A., and Li, M. (1999). The biogeography of C4 photosynthesis: patterns and controlling factors. In: ‘Plant Biology’. (Eds R. F. Sage and R. K. Monson.) pp. 313–373. (Academic Press: San Diego, CA.)

Scheiter, S., Higgins, S. I., Osborne, C. P., Bradshaw, C., Lunt, D., Ripley, B. S., Taylor, L. L., and Beerling, D. J. (2012). Fire and fire-adapted vegetation promoted C4 expansion in the late Miocene. New Phytologist 195, 653–666.
Fire and fire-adapted vegetation promoted C4 expansion in the late Miocene.CrossRef | 22712748PubMed |

Senft, R., Coughenour, M., Bailey, D., Rittenhouse, L., Sala, O., and Swift, D. (1987). Large herbivore foraging and ecological hierarchies. Bioscience 37, 789–799.
Large herbivore foraging and ecological hierarchies.CrossRef |

Sierra, J., Brisson, N., Ripoche, D., and Deque, M. (2010). Modelling the impact of thermal adaptation of soil microorganisms and crop system on the dynamics of organic matter in a tropical soil under a climate change scenario. Ecological Modelling 221, 2850–2858.
Modelling the impact of thermal adaptation of soil microorganisms and crop system on the dynamics of organic matter in a tropical soil under a climate change scenario.CrossRef | 1:CAS:528:DC%2BC3cXht1ems7zL&md5=f6aaaa7b647bc0dabcc63634a5910d17CAS |

Sinninghe Damsté, J. S., Verschuren, D., Ossebaar, J., Blokker, J., van Houten, R., van der Meer, M. T., Plessen, B., and Schouten, S. (2011). A 25,000-year record of climate-induced changes in lowland vegetation of eastern equatorial Africa revealed by the stable carbon-isotopic composition of fossil plant leaf waxes. Earth and Planetary Science Letters 302, 236–246.
A 25,000-year record of climate-induced changes in lowland vegetation of eastern equatorial Africa revealed by the stable carbon-isotopic composition of fossil plant leaf waxes.CrossRef |

Snyder, K. A., and Tartowski, S. L. (2006). Multi-scale temporal variation in water availability: implications for vegetation dynamics in arid and semi-arid ecosystems. Journal of Arid Environments 65, 219–234.
Multi-scale temporal variation in water availability: implications for vegetation dynamics in arid and semi-arid ecosystems.CrossRef |

Su, P. X., Xie, T. T., and Zhou, Z. J. (2011). C4 plant species and geographical distribution in relation to climate in the desert vegetation of China. Sciences in Cold and Arid Regions 3, 381–391.

Tang, H. P., and Liu, S. R. (2001). The list of C4 plants in the Inner Mongolia area. Journal of Inner Mongolia University 4, 431–438.

Teeri, J., and Stowe, L. (1976). Climatic patterns and the distribution of C4 grasses in North America. Oecologia 23, 1–12.

Tooth, I. M., and Leishman, M. R. (2013). Post-fire resprouting responses of native and exotic grasses from Cumberland Plain Woodland (Sydney, Australia) under elevated carbon dioxide. Austral Ecology 38, 1–10.
Post-fire resprouting responses of native and exotic grasses from Cumberland Plain Woodland (Sydney, Australia) under elevated carbon dioxide.CrossRef |

Wand, S. J., Midgley, G., Jones, M. H., and Curtis, P. S. (1999). Responses of wild C4 and C3 grass (Poaceae) species to elevated atmospheric CO2 concentration: a meta-analytic test of current theories and perceptions. Global Change Biology 5, 723–741.
Responses of wild C4 and C3 grass (Poaceae) species to elevated atmospheric CO2 concentration: a meta-analytic test of current theories and perceptions.CrossRef |

Wang, R. (2002). Photosynthetic pathway types of forage species along a grazing gradient from the Songnen grassland, Northeastern China. Photosynthetica 40, 57–61.
Photosynthetic pathway types of forage species along a grazing gradient from the Songnen grassland, Northeastern China.CrossRef |

Wang, S. P., Li, Y. H., and Wang, Y. F. (1999). Relationship between foraging areas of sheep and spatial heterogeneity of grassland landscape. Acta Ecologica Sinica 19, 431–436.

Wang, S. P., Wang, Y. F., and Chen, Z. Z. (2003). Effect of climate change and grazing on populations of Cleistogenes squarrosa in Inner Mongolia steppe. Acta Phytoecologica Sinica 27, 337–343.

Waters, C. M., Garden, D. L., Smith, A. B., Friend, D. A., Sanford, P., and Auricht, G. C. (2005). Performance of native and introduced grasses for low-input pastures. 1. Survival and recruitment. The Rangeland Journal 27, 23–39.
Performance of native and introduced grasses for low-input pastures. 1. Survival and recruitment.CrossRef |

Way, D. A. (2012). What lies between: the evolution of stomatal traits on the road to C4 photosynthesis. New Phytologist 193, 291–293.
What lies between: the evolution of stomatal traits on the road to C4 photosynthesis.CrossRef | 1:CAS:528:DC%2BC38XitVejs7w%3D&md5=f03b612d09f3b8796026dd641a9caa5fCAS | 22221147PubMed |

Whalley, R. D. B. (1994). State and transition models for rangelands 1. Successional theory and vegetation change. Tropical Grasslands 28, 195–205.

Wittmer, M., Auerswald, K., Bai, Y. F., Schaufele, R., and Schnyder, H. (2010). Changes in the abundance of C3/C4 species of Inner Mongolia grassland: evidence from isotopic composition of soil and vegetation. Global Change Biology 16, 605–616.
Changes in the abundance of C3/C4 species of Inner Mongolia grassland: evidence from isotopic composition of soil and vegetation.CrossRef |

Wu, J., and Loucks, O. (1995). From balance of nature to hierarchical patch dynamics: a paradigm shift in ecology. The Quarterly Review of Biology 70, 439–466.
From balance of nature to hierarchical patch dynamics: a paradigm shift in ecology.CrossRef |

Yokohama, M., Shimada, S., Sekiyama, A., Gombojav, A., and Ariunsren, P. (2011). Grassland vegetation and palatability in Mongolian grasslands. Journal of Agricultural Science - Tokyo Nogyo Daigaku 56, 203–211.

Zech, M., Zech, R., Morras, H., Moretti, L., Glaser, B., and Zech, W. (2009). Late Quaternary environmental changes in Misiones, subtropical N-E Argentina, deduced from multi-proxy geochemical analyses in a palaeosol-sediment sequence. Quaternary International 196, 121–136.
Late Quaternary environmental changes in Misiones, subtropical N-E Argentina, deduced from multi-proxy geochemical analyses in a palaeosol-sediment sequence.CrossRef |

Zhang, Z., Zhao, M., Lu, H., and Faiia, A. M. (2003). Lower temperature as the main cause of C4 plant declines during the glacial periods on the Chinese Loess Plateau. Earth and Planetary Science Letters 214, 467–481.
Lower temperature as the main cause of C4 plant declines during the glacial periods on the Chinese Loess Plateau.CrossRef | 1:CAS:528:DC%2BD3sXnt1CgtLg%3D&md5=c73824217852bf575caf32da33e7bb69CAS |

Zheng, S., Lan, Z., Li, W., Shao, R., Shan, Y., Wan, H., Taube, F., and Bai, Y. (2011). Differential responses of plant functional trait to grazing between two contrasting dominant C3 and C4 species in a typical steppe of Inner Mongolia, China. Plant and Soil 340, 141–155.
Differential responses of plant functional trait to grazing between two contrasting dominant C3 and C4 species in a typical steppe of Inner Mongolia, China.CrossRef | 1:CAS:528:DC%2BC3MXitFGks7k%3D&md5=a7e393afb0fff8ef7011a67e1d67cef9CAS |


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