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

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

Terrestrial vegetation is composed of 95% C₃ plants and 5% C₄ plants (Su et al. 2011), but C₄ plants contribute about 20% of global gross primary productivity (Wand et al. 1999). The C₄ pathway of photosynthesis in the dicots originated in arid regions at low latitudes and C₄ grasses and sedges dominate nearly all grasslands in the tropics, subtropics and warm temperate zones and are major components of arid landscapes from the temperate regions to the tropics (Archibold 1995; Sage et al. 1999). The relative abundance of C₄ plants is not only an aspect of ecosystem structure, but more importantly, it reflects ecosystem functions (Snyder and Tartowski 2006; Sierra et al. 2010). Thus, studies on the relative abundance of C₄ plants have become more important in the context of global climate change (Kohn 2010; Wittmer et al. 2010; Scheiter et al. 2012).

The concentration of CO₂ in the atmosphere, air temperature, and land-use patterns are generally considered to be the main drivers that influence the relative abundance of C₄ and C₃ species (Zech et al. 2009; Pushkina et al. 2010; Wittmer et al. 2010). Compared with C₃ plants, C₄ plants have higher water-use efficiency and greater photosynthetic rates at low atmospheric CO₂ concentrations resulting in greater growth under these conditions (Farquhar et al. 1989; Leegood 2013). A series of studies on paleoclimate climate modelling, and vegetation changes have confirmed the fact that the relative abundance of C₄ plants will decrease with increasing atmospheric CO₂ concentration (Cerling et al. 1993; Scheiter et al. 2012; Ripley et al. 2013). However, some studies did not fully support this view (Owensby et al. 1999; Tooth and Leishman 2013). Then researchers gradually realised the importance of temperature. On one hand, C₄ plants appear only if the temperature is above a certain threshold (Teeri and Stowe 1976; Sage 2004). The optimum temperatures for many C₄ species are about 35°C and at temperatures lower than about 15°C, the growth of most C₄ species virtually stops. The optimum for many C₃ species is about 20−25°C and growth will continue down to close to 0°C (McWilliam 1978). On the other hand, a temperature rise would directly affect the relative C₃ and C₄ plant growth and dry matter accumulation and would ultimately determine the relative abundance of the two groups in the vegetation (Sage and Kubien 2007; Wittmer et al. 2010).

Disturbance, including grazing, fire, and roads related to land-use change, also have different effects on the growth and reproduction of C₃ and C₄ plants and can lead to changes in their relative abundance (Pushkina et al. 2010; Collins and Calabrese 2012; Scheiter et al. 2012; Way 2012). Animal grazing is the most dominant land use of grasslands (Mavromihalis et al. 2013). Grazing influence on the relative abundance of C₄ plants has received much attention in the study of grasslands in North and South America (Reeder et al. 2004; Altesor et al. 2006; Derner et al. 2006), Central Asia (Auerswald et al. 2012; Ren et al. 2012), South Africa (Franz-Odendaal et al. 2002), Australia (Bell et al. 2012) and New Zealand (Crush and Rowarth 2007). Most of these studies suggest that grazing increases the relative abundance of C₄ species in some plant communities (Reeder et al. 2004; Waters et al. 2005; Fanselow et al. 2011). Two reasons may explain these results. Firstly, grazing may have changed the micro-environment. Secondly, the foraging preferences of herbivores caused by the different palatability of C₃ and C₄ plants (McPherson and Rasmussen 1989), as well as differences in their digestibility could mean that the animals select either C₃ or C₄ plants (Whalley 1994; Norman et al. 2009). However, other studies suggested that grazing had no effects on the relative abundance of C₄ plants (Derner et al. 2006; Auerswald et al. 2012).

Since the household is the basic management unit of the grasslands in Inner Mongolia (Hou et al. 2012), the objective of the present work was to understand the relative importance of grazing and temperature in determining the relative abundance of C₄ plants in these grasslands at this scale. Bearing in mind that temperature may affect the relative abundance of C₄ plants at a large temporal-spatial scale, grazing may play a more important role at a smaller temporal-spatial scale (Franz-Odendaal et al. 2002; Reeder et al. 2004; Bell et al. 2012).

We hypothesise that, at the household scale, grazing is the primary driver for the changes in the relative abundance of C₄ plants in grassland communities in Inner Mongolia. To verify this hypothesis, we selected 32 households in the Baiyinxile ranch, located in a typical steppe grassland region in Inner Mongolia, and monitored the relative abundance of C₄ plants during 2008–12. We also determined the mean annual temperature and grazing intensity at each household, and analysed the effects of these two factors and their combinations on the relative abundance of C₄ plants. This study aimed to enrich the understanding of the changes in the relative abundance of C₃ and C₄ plants in response to environmental factors, and provide a better basis for assessing the effects of climate and land-use change on grassland ecosystem structure and functioning, and provide support for the development of improved management strategies.

This study was conducted on the Baiyinxile ranch, Xilingol league of Inner Mongolia (Fig. 1), ranging from 116.03°E to 116.79°E and 43.69°N to 44.27°N. Gentle hills and high plains constitute the major terrain with altitude ranging from 1126 m to 1384 m above mean sea level. It is a temperate continental climate, characterised by a mean annual temperature of –0.1°C, and mean annual precipitation of 350 mm. The main soil type is a chestnut soil. The region is covered by typical steppe vegetation with Stipa grandis P.Smirn. and Leymus chinensis (Trin.) Tzvel. as the major dominant species. The ‘double rights one system’ land policy began in 1999 and was fully implemented in 2003. It is the semi-private property rights, which mean that both the livestock and grassland are contracted to herder households, but the grasslands belong to the state (Li et al. 2007). Thus, individual households became the basic production and management units at that time. The most common grazing animals were sheep, goats and cattle in this area.

Fig. 1.  Location map of Inner Mongolia showing the study region (Xilingol league), the Baiyinxile ranch and the sampling sites.

Vegetation data were collected from 2008 to 2012 between the end of July and mid-August when the aboveground biomass is at its peak. The grasslands within 32 households (all with long-term grazing from 2003) were investigated. In each household, an area of 10 × 10 m was selected and monitored during the whole period. The grasslands at all these sites were dominated by Stipa species (S. grandis or S. krylovii Roshev). The grazing intensity at each site was estimated based on the distance of the site from the housing and sheepfolds, that is, a greater intensity was estimated for sites close to the housing and sheepfolds. The average distance of a site from housing was 500 m (An and Han 2011). Since topography, grassland community type and plant patches all affect the foraging behaviour of sheep (Senft et al. 1987), we selected the monitoring site within each household to ensure that the selected site was representative of the average grazing intensity within the household. Each site was selected (Wang et al. 1999) on flat land and in an area where the vegetation reflected, as much as possible, the overall vegetation condition of the household and having the lowest heterogeneity. All sites were located with a global positioning system device. At peak plant biomass, three 1 × 1-m plots were randomly placed at each site to determine aboveground plant biomass by harvesting species by species and drying at 65°C (for ~24 h) in the laboratory. Each year, care was taken to ensure that the new sampling sites were not at the same locations that had been previously sampled. All species were grouped into C₃ or C₄ species (Tang and Liu 2001), and the relative abundance of C₄ species was calculated as their proportion of the total aboveground biomass of the grassland at each site. The monitoring of vegetation on all the 32 sites lasted for 5 years, and during this period, six C₄ species were recorded: Artemisia sieversiana Ehrhart ex Willd., Cleistogenes squarrosa (Trin.) Keng, Chenopodium aristatum L., Ch. glaucum L., Kochia prostrata (L.) Schrad. and Salsola collina Pall. and 53 C₃ species were recorded.

The vegetation monitoring started in 2008, but portable weather stations (Kestrel 4500, USA) were not established on the 32 sites until 2012. The mean annual temperature data for 2012 were obtained from these portable weather stations, whereas the information for 2008–11 was derived from the nearby Xilingol meteorological station. All the sites were within 40 km of this station but at different altitudes. The established adiabatic lapse rate is –0.6°C 100 m^–1, so the mean annual temperature at each site was estimated using following formula:

where T_s and A_S are the annual mean temperature and altitude at a site, and T_m (^oC) and 1226.4 m are the annual mean temperature and altitude, respectively, at Xilinhot meteorological station.

The accuracy of these calculations was verified by comparing the estimated values for 2012 against that recorded by the portable weather stations. The correlation between the estimated and recorded data across the 32 sites was significant (P < 0.01) and indicated the high reliability of the calculation method (Fig. 2).

Fig. 2.  The relationship between observed mean annual temperature using portable weather stations and the model-estimated mean annual temperature based on the altitude of the studied sites and data from the Xilingol meteorological station.

We calculated the grazing intensity at each of the 32 households for each year, using the pasture area divided by standardised sheep units (SU). The average distance of a site from housing, sheepfolds or a water-point was 500 m. Therefore, we can minimise the error caused by the distance to grazing intensity. The number of different livestock at each household were surveyed along with the vegetation survey each year, and were converted into the number of SU based on their feed requirements (Li and Ji 2004), i.e. for cattle, horses, or mules, 1 animal = 5 SU, and 1 lamb = 0.5 SU.

The sensitivity of C₃ plants, C₄ plants and each of the six C₄ species to environmental factors was tested by calculating the coefficient of variation (CV) of their aboveground biomass across the 32 households from 2008 to 2012. We also calculated Pearson correlation coefficients between grazing intensity, mean annual temperature, and the relative abundance of all and each of the six C₄ species. To examine the effect of temperature and grazing on the relative abundance of C₄ plants, four different detrended canonical correspondence analyses (DCCA) were run based on Borcard points (Borcard et al. 1992) using three matrices of data of the relative abundance of C₄ plants, mean annual temperature and grazing intensity (each matrix consisted of 32 households and 5 years). The separate and coupled effect of temperature and grazing, as well as the effects of all other factors on the relative abundance of C₄ plants, were assessed using the ratio of the total variation of the relative abundance of C₄ plants to the variation of temperature, grazing intensity, temperature × grazing intensity, or all other factors. That is, we first calculated the effect of temperature (Et) and grazing intensity (Eg) on the relative abundance of C₄ plants using the constrained ordination analysis with temperature or grazing intensity, respectively, as the constrained factor. Then we calculated the effect of only temperature (Et0) and only grazing intensity (Eg0) by the same approach after exclusion of the effect of grazing (with grazing intensity as a co-variable) or the effect of temperature (with temperature as a co-variable), respectively. Based on these calculations, the coupling effect between temperature and grazing was calculated as (Et-Et0) or (Eg-Eg0), and the effect of all other factors was 1 – (Et + Eg0) or 1 – (Et0 + Eg).

All statistical analyses were performed using SPSS 17.0 and Canaco 4.5 (Braak and Smilauer 2002).

Averaged over all 32 sites, the percentage of C₃ plants in the plant biomass was 87.7% (Fig. 3). The contribution of C₄ plants to community biomass decreased from 28.2% in 2008 to 6.9% in 2012, and was 12.3% on average.

Fig. 3.  The proportion of C₃ (dark shading) and C₄ (light shading) plants in the aboveground biomass of grassland from 2008 to 2012.

We calculated the CV of aboveground biomass of C₃ and C₄ plants at the 32 sites from 2008 to 2012. The CV of C₄ plants (69%) was greater than that of C₃ plants (53%) (Fig. 4). There were also differences in CV among the six C₄ species: C. squarrosa, Ch. aristatum, Ch. glaucum and S. collina had a higher CV, while A. sieversiana and K. prostrata had a lower CV. The lower CV of these latter two species was mainly related to their lower frequency in the studied grasslands. Artemesial sieversiana only appeared at two sites in 2009 and 2011, and K. prostrata appeared at three sites in 2008, 2009 and 2012.

Fig. 4.  The coefficients of variation of all C₃ plants, all C₄ plants and six C₄ species: Cleistogenes squarrosa (Trin.) Keng, Chenopodium aristatum L., Ch. glaucum L., Salsola collina Pall., Artemisia sieversiana Ehrhart ex Willd., and Kochia prostrata (L.) Schrad. across 32 grassland sites during 2008–12.

The relative abundance of all the C₄ plants showed a positive correlation with grazing intensity and with mean annual temperature across the 32 households (Fig. 5a1, a2). The relative abundance of C. squarrosa, Ch. glaucum, and S. collina was also significantly correlated with grazing intensity or mean annual temperature, respectively (Fig. 5b1, c1, d1, b2, c2 and d2). These results showed that the relative abundance of these three C₄ species was higher with a high grazing intensity and a high mean annual temperature.

Based on four different DCCA analyses, we determined the separate effects of temperature alone, grazing intensity alone and the coupling effects of temperature and grazing intensity, as well as the effects of all other factors on the variation in the relative abundance of C₄ species (Table 1). Grazing intensity explained 53.6% of the variation, among which 41.1% was explained by grazing intensity alone. Temperature explained 42.6% of the variation, and 30.1% of which was explained by temperature alone. Only 12.5% of the variation was explained by the coupled effects of temperature and grazing; and all other factors explained the rest (16.3%). Thus grazing and temperature together led to the differences in relative abundance of C₄ species, and the effects of grazing was greater than those of temperature.

Table 1.  Results of detrended canonical correspondence analyses and partitioning of the variation of the relative abundance of C₄ plants among different variables

It is widely considered that higher temperatures are generally associated with greater abundance of C₄ plants (Zheng et al. 2011; Auerswald et al. 2012). Our data supported this statement in that there was a decrease in the abundance of C₄ species associated with a decrease in temperature over the years 2008–12 (Figs 3 and 5a2). This is because C₄ species have a competitive advantage in environments with higher temperatures, lower CO₂ concentrations, higher solar radiation, and lower soil moisture contents (Sage and Kubien 2007). The rising temperatures and associated climatic aridity predicted by climate-change scenarios (Kang et al. 2011) are therefore likely to lead to an increase in the abundance of C₄ species in the Inner Mongolia grasslands.

Although there is some dispute about whether grazing can affect the relative abundance of C₄ plants (Derner et al. 2006; Fanselow et al. 2011), a series of studies carried out in the Inner Mongolian steppe have found that grazing intensity can indeed increase the relative abundance of C₄ plants (Wang 2002; Fanselow et al. 2011; Zheng et al. 2011). Our results at the household scale also support these earlier findings (Fig. 5). Three reasons may explain these results. Firstly, grazing suppresses C₃ plants more than C₄ plants and C₄ plants turn generally green later than C₃ plants (by 6 weeks, see Liang et al. 2002), and thus avoid grazing damage in early spring. In addition, C₄ species (mainly C. squarrosa) also have a lower canopy (<10 cm) than C₃ plants (20–50 cm) and thus avoid being grazed by cattle (Wang et al. 2003). Secondly, removal of the biomass of C₃ plants through grazing enhances the intensity of light reaching the ground and the action of wind, creating a drier and warmer micro-environment (Teeri and Stowe 1976; Li et al. 2000), which facilitates the development of C₄ plants (Sage 2004). The shade from tall C₃ plants not only reduces the light availability for short grasses, but also changes the proportion of infrared/far-infrared (Casal et al. 1987). Controlled experiments have demonstrated that the proportional reduction of infrared/far-infrared light can reduce the tillering of C. squarrosa (Deregibus et al. 1985; Casal et al. 1987), the major C₄ species in the studied grassland. Infrared light intensity diminishes to a greater extent than far-infrared when light is filtered through the plant canopy, thus removal of the upper plant canopy by grazing will increase the infrared/far-infrared ratio of the light reaching the short grasses, and will enhance the tillering of C. squarrosa. The last and perhaps the most important reason is the differences in the preference (McPherson and Rasmussen 1989) and digestibility (Norman et al. 2009) of the C₃ and C₄ species. Yokohama et al. (2011) reported that the species most preferred by grazing livestock on the Mongolian plateau [S. glareosa, P. smirnov, S. krylovii, Achnatherum splendens (Trin.) Nevski, Agropyron cristatum (L.) Gaertn., Elytrigia repens (L.) Nevski, L. chinensis, Poa pratensis L., Artemisia frigid Willd., and Caragana pygmaea (L.) DC. etc.] are all C₃ species. These species maintain the forage production of Inner Mongolian grasslands. The results of Norman et al. (2009) indicated that the C₄ species in the region have lower digestibility values than C₃ species and so the grazing livestock tend to prefer the C₃ species.

Fig. 5.  Changes in the relative abundance of all C₄ plants plus the relative abundance of three individual C₄ species in the aboveground biomass with increasing grazing intensity or increasing mean annual temperature at the Baiyinxile ranch, Inner Mongolia.

Scale is widely considered to be the main cause of differences among ecological models because of the operation of different mechanisms at different scales (Wu and Loucks 1995). Temperature is the most important factor in the evolution of paleoclimates (Zhang et al. 2003; Pushkina et al. 2010) and the change in relative abundance of C₄ plants on a large scale (Sage 2004; Wittmer et al. 2010). Auerswald et al. (2012) found that C₄ abundance in an Inner Mongolia grassland system is driven by a temperature-moisture interaction, not grazing pressure. Our study shows that grazing had a greater effect than temperature in altering the abundance of C₄ plants at the small scale across households, which is in agreement with similar conclusions in other studies (Fanselow et al. 2011). Scale must be taken into account when defining the relative effects of different factors on ecological processes and functions, including the effects on the abundance of C₄ plants.

However, our results are different from those of Auerswald et al. (2012). In their study, the temporal variation in the abundance of C₄ plants was measured at one site that experiences large inter-annual variation in climate (temperature as well as precipitation) but under a small range of grazing intensities (02.25 SU ha^–1), while our study considered the spatial variation in the abundance of C₄ plants on grasslands across 32 households, where the variation in mean annual temperature was small, and the range of grazing intensities was large (0–5.25 SU ha^–1). The contrasting results of Auerswald et al. (2012) and ours indicate that the relative importance was dependent on the relative scales of the different factors. For the same group of factors, those with more variation would have greater effects than those with less variation.

Changes in a range of environmental factors, including grazing, temperature, road construction and precipitation, at both large scale and small scales, can affect changes in the biomass of C₄ plants (Jolly and Haxeltine 1997; Pushkina et al. 2010; Sinninghe Damsté et al. 2011; Collins and Calabrese 2012; Scheiter et al. 2012; Way 2012). In our study, the CV of C₄ species was higher than that of C₃ species (Fig. 4) implying that C₄ plants exhibited a greater sensitivity to environmental change than the C₃ plants. In particular, three C₄ species: C. squarrosa, C. glaucum, and S. collina, not only showed more sensitivity to environmental change (Fig. 4), but they also all showed an increasing abundance with increased grazing pressure and temperature (Fig. 5). Thus, the changes in the abundance of these species could be used as indicators for detecting climate change and human disturbance in Inner Mongolian grasslands.