Fiber fractions, multielemental and isotopic composition of a tropical C₄ grass grown under elevated atmospheric carbon dioxide

Introduction

Fossil fuel combustion, land use changes, and the expansion of population and industry have significantly contributed to the global carbon dioxide (CO₂) rise, from the preindustrial level of 280 ppm to the current level of 400 ppm (International Panel on Climate Change (IPCC)—Climate Change, 2014; Broberg, Högy & Pleijel, 2017), and this increase is expected to continue. According to the representative concentration pathways (RCPs) of International Panel on Climate Change (2014), the atmospheric CO₂ concentration is estimated to reach the range of 420 ppm (RCP2.6) to 1,300 ppm (RCP8.5) in the next decades. Such increases in CO₂ concentration is expected to have cascading effects on numerous aspects of plant biochemistry, since plant productivity is strongly tied to atmospheric CO₂ through photosynthesis (Dietterich et al., 2015).

Experimental studies simulating future scenarios predict that C₄ species are less responsive to elevated CO₂ conditions in comparison with C₃ species due to the differences in their photosynthetic mechanism (Ehleringer & Björkman, 1977; Sage & Kubien, 2007; Reich et al., 2018). C₄ species have a C-accumulation strategy, which minimizes photorespiration through biochemical and anatomical specializations. Using this strategy, C₄ species can concentrate CO₂ at the active site of the ribulose-1,5-bisphosphate carboxylase-oxygenase (RuBisCO) (Sage, 2004) and be virtually CO₂ saturated even at the current atmospheric CO₂ concentration (Tom-Dery et al., 2018). In addition, photosynthetic capacity of many plant species reduced, when they were exposed to elevated CO₂ due to an inhibition mechanism called photosynthetic acclimation, generally attributed to an alteration in the balance of the supply and sink of assimilates leading to increased nonstructural carbohydrates content in the leaves (Drake, González-Meler & Long, 1997; Porras et al., 2017). However, indirect effects of elevated CO₂ can increase leaf CO₂ assimilation rate and growth of C₄ species via increases in intracellular partial pressure, changes in fixation patterns, improvements of shoot water relations, and increases in leaf temperature (Ghannoum et al., 2000). In addition, recent results from a 20-year free air carbon dioxide enrichment (FACE) experiment showed a much more positive response of C₄ species to elevated atmospheric CO₂ concentration compared to C₃ grasses after 12 years of exposure (Reich et al., 2018).

The response of grasslands to climate change is complex due to the interactions between water availability and management practices (Chang et al., 2017). Higher concentrations of atmospheric CO₂ have the potential to alter food and fodder nutritional quality (Porteaus et al., 2009; Abdelgawad et al., 2014; Myers et al., 2014; Dumont et al., 2015). Some authors have already noticed that elevated CO₂ can improve pasture productivity at the expense of a decreased nutritional quality of forage (Milchunas et al., 2005; Mueller et al., 2016; Augustine et al., 2018) and this could result in low production and reproduction rates of grazing livestock since these animals usually depend exclusively on forages to meet their nutritional requirements (Ezzat, Fadlalla & Ahmed, 2018).

Changes in production and chemical composition of plants have significant impact on ecological processes (Damatta et al., 2010; Sanz-Sáez et al., 2012; Abdelgawad et al., 2014). Effects of CO₂ enrichment on plants have been intensively investigated in C₃ species (Lara & Andreo, 2011), but some recent studies have investigated these effects on tropical C₄ grasses (McGranahan & Yurkonis, 2018; Santos et al., 2014; Tom-Dery et al., 2018). These C₄ grasses are the main fodders in the Brazilian livestock production system, having the largest commercial herd of ruminants with nearly 211 million head (15% of world’s beef production) in an area of approximately 170 million hectares of grasslands (Instituto Brasileiro de Georgrafia e Estatística, 2012; Barneze et al., 2014; Dick, Da Silva & Dewes, 2015; Cerri et al., 2016). Most of this area is under native African C₄ grass species, mostly belonging to the genus Brachiaria (Gracindo et al., 2014). Although the livestock sector in Brazil is one of the largest in the world, little information is available regarding the changes in pasture productivity and forage nutritional quality due to enhanced atmospheric CO₂.

Therefore, the main objective of this study was to investigate changes in pasture productivity and forage nutritional quality of Brachiaria decumbens (cv. Basilisk) in response to 30-month exposure to elevated atmospheric CO₂. We hypothesized that elevated concentration of atmospheric CO₂ may result in increased pasture productivity, changes in morphological characteristics and changes in nutritional quality of the forages.

Materials and Methods

Study site and FACE facility

This experiment was carried out in an experimental area belonging to the Brazilian Agricultural Research Corporation (Embrapa—Meio Ambiente) located in the municipality of Jaguariúna (22°43′S, 47°01′W, 570 m a.s.l), State of São Paulo, Brazil. According to the Köppen classification, the climate is humid subtropical (Cfa), with hot rainy summers and cold dry winters (Fig. 1). The soil is classified as dystrophic Red Latosol with clayey texture, according to the Brazilian soil classification system. Soil physico-chemical properties of the site are described in Maluf et al. (2015).

A total of 12 octagonal rings with 10 m diameter were established in a seven-ha coffee plantation (Coffea arabica cv. Catuaí vermelho IAC 144) and forage growth was investigated in a FACE experiment. Six rings were considered as control under normal atmospheric CO₂ (390 μmol mol⁻¹ CO₂; δ¹³C = −8‰) and the other six rings were under elevated atmospheric CO₂ (550 μmol mol⁻¹ CO₂; δ¹³C = −10.6‰). The level of atmospheric CO₂ concentration in elevated atmospheric CO₂ treatments was increased with an arrangement of tubes and wireless network controlled by environmental sensors (WXT520 climate sensor and GMM343 CO₂ sensor from Vaisala Co., Helsinki, Finland) through the injection of pure CO₂ (δ¹³C = −30.7‰) as described by Ghini et al. (2015). CO₂ enrichment was began in August 2011. The level used in this study (550 μmol mol⁻¹ CO₂) is based on the intermediate scenario (RCP6.0) by 2,070 (International Panel on Climate Change, 2013) and have already affected some crops (McGranahan & Poling, 2018).

Results

Elevated CO₂ had no effect on biomass productivity, average height, and proportions of leaf, stem, senescence, and inflorescence (Table 1). The OM and fiber fractions of the whole forage, leaf, stem, and senescence portions were also not influenced by elevated CO₂ concentration (Table 2). Elevated CO₂ showed a nonsignificant (p > 0.05) 18% decrease in biomass productivity, 10% decrease in average height, 4% decrease in FDAom and 5% decrease in Lignin (sa) related to control.

Despite no significant effect on C and N concentrations, a decrease (p < 0.05) in the C:N ratio of the whole plant was observed under elevated CO₂ (Table 3). In addition, elevated CO₂ led to higher values of δ¹⁵N in the leaf and stem portions of B. decumbens (p < 0.05). However, such increase (0.4‰ and 0.7‰ in leaf and stem portions, respectively) was generally lower or very close to 0.5‰, which is the analytical error of this analysis.

Elevated CO₂ did not influence the concentrations of K, S, P, Fe, and Mn in the whole plant, leaf, stem, and senescent portions (Figs. 2A–2E). However, lower concentration of Ca was observed in the leaf (12%) and senescence portion (18%) of B. decumbens grown under elevated atmospheric CO₂ (p < 0.05) (Fig. 2F).

Discussion

Even after two and half years of exposure to elevated atmospheric CO₂ concentration, the productivity, and morphological characteristics of B. decumbens (cv. Basilisk) were not influenced, following the same pattern observed in our trial with B. brizantha (cv. Marandu) in a short term (9 months) experiment (A. L. Abdalla Filho, P. M. T. Lima, G. Z. Sakita, T. P. D. Silva, W. S. Costa, R. Ghini, A. L. Abdalla, M. C. Piccolo, 2019, unpublished data). These results rejects our initial hypothesis and are in line with Dumont et al. (2015) stating that only N content and nonstructural carbohydrates concentrations increased under elevated CO₂ in a meta-analysis. No effects of elevated CO₂ (950 μmol mol⁻¹ CO₂) on total biomass of the C₄ grass Cenchrus pedicellatus were also observed by Tom-Dery et al. (2018). However, a recent study conducted over 20 years in a FACE facility in Minnesota, USA, showed that after 12 years of exposure to elevated CO₂, the total biomass of several C₄ grasses enhanced (Reich et al., 2018). Effects of elevated CO₂ could also vary according to the evaluated cultivar. Using growth chambers and the same concentration level of our study (550 μmol mol⁻¹ CO₂), Santos et al. (2014) evaluated three cultivars of buffel grass (Cenchrus ciliaris) and found that elevated CO₂ did not affect the productive characteristics of Biloela, decreased Aridus forage mass and increased forage mass in West Australia. The reason for discrepancies between different studies is unknown but it is important to consider the differences in methodologies as a possible explanation (McGranahan & Yurkonis, 2018) since growth chambers may overestimate the effects of elevated CO₂ on photosynthetic and plant growth parameters (Leakey et al., 2006).

Plants respond directly to higher atmospheric CO₂ concentration through photosynthesis and stomatal conductance, and these are the basis for the higher biomass production (Long et al., 2006). However, in C₄ plants, RuBisCO is localized in bundle sheath cells, in which CO₂ is concentrated in levels of three to six times higher than those of the atmospheric CO₂ concentration (Caemmerer & Furbank, 2003). Such CO₂ enrichment is sufficient to saturate RuBisCO and prevent any increase in CO₂ uptake with CO₂ fertilization. In addition, under elevated CO₂ condition, C₄ plants can close their stomata to reduce water loss during photosynthesis (McGranahan & Poling, 2018). Still, sufficient rainfall during the experimental period (Fig. 1) could limit gains from reduced transpiration (Fay et al., 2012). For these reasons and the fact that we used a FACE facility, we observed the lack of response to elevated CO₂ in our study.

Structural carbohydrates in B. decumbens were also not affected by the increased atmospheric CO₂ concentration, refuting our hypothesis. These results are in line with Dumont et al. (2015) but contradicts the findings of Abdalla et al. (2016) evaluating this cultivar under the same treatments (control and elevated CO₂) during the rainy season. Our results also contradict Tom-Dery et al. (2018) stating that elevated CO₂ reduced Lignin and increased ADF content of Cenchrus pedicellatus. It is noteworthy that in our study, in order to evaluate the effect of 30 month exposure to elevated atmospheric CO₂, the grass was kept under no grazing management (e.g., considering the concept of critical leaf area index to determine the time of sampling) for almost 6 months, which resulted in older plants with higher proportion of stem, as well as fiber fractions compared to the other studies evaluating the same cultivar (Pedreira, Braga & Portela, 2017; Lima et al., 2018).

By altering plant and microbial processes involved in the N cycle, elevated atmospheric CO₂ may change the isotopic signature of plant N (Polley et al., 2015). In our study, a slightly lower C:N ratio was found when the whole plant was analyzed (Table 3). Similarly, rather higher δ¹⁵N values were found under elevated CO₂ in some plant parts. In another study, higher δ¹⁵N in leaves of ponderosa pine with increasing atmospheric CO₂ was recorded (Johnson, Cheng & Ball, 2000); meanwhile, in our study the difference was significant but it was too small to be attributed to elevated CO₂.

The major difference was a reduced Ca content of the leaves and the senescence portion of B. decumbens under elevated atmospheric CO₂. Calcium is an essential macronutrient for plant growth, plays an important structural role in the cell wall and membranes, and acts as an intracellular messenger in the cytosol (White & Broadley, 2003). Lower levels of Ca in forage may have implications for animal nutrition since reduced availability of Ca to the rumen microbes decreases fiber digestion (Fielding & Miller, 1986). The Ca content of forages is the net result of absorption and translocation processes operating within the roots and shoots and such processes are being modulated by various environmental factors affecting plant growth and metabolism (Grunes & Welch, 1989).

Other studies found lower Ca concentration in sorghum and soybean under elevated atmospheric CO₂ due to the dilution effect caused by an increased biomass (Rogers, Runion & Krupa, 1994; Rogers et al., 1999), often referred as the “dilution hypothesis” (Loladze, 2014). As the yield was not changed due to the elevated CO₂ in our study, other mechanisms may be involved in reduced Ca concentration. Related to the flow of nutrients, the processes involved in the use of available water may be affected by elevated CO₂ concentration since under this condition, transpiration rates of plants may be reduced and water use efficiency in photosynthetic processes may be improved (Fay et al., 2012). In this study, the plots were kept under similar soil fertility, daily air temperature and rainfall conditions, and the only different parameter was the concentration of atmospheric CO₂, hence the reduced Ca content under elevated CO₂ is more related to an enhanced water use efficiency (parameter not evaluated here) rather than the dilution hypothesis. Despite the reduced Ca content of B. decumbens under elevated CO₂, it is important to emphasize that a possible Ca deficiency in ruminants can be easily ameliorated by feeding calcium-containing mineral supplements (e.g., limestone, steamed bone flour, and dicalcium phosphate) (McDonald et al., 2011).

The predicted world population of 9.6 billion in the next decades will result in 70% increase in the demand of animal derived foods and considering the current scenario of climate change, sustainable production of them to achieve food security will be a big challenge faced by humanity (Gerber et al., 2013; Cerri et al., 2016). Our results showed that the productivity and fiber fractions of B. decumbens were not impaired by elevated CO₂, suggesting that the tropical pasture-based beef production has the potential to overcome the above-mentioned challenges. A remarkable sustainable potential of grazing systems is also shown in recent studies (De Oliveira Silva et al., 2016; Dass et al., 2018).

Conclusions

We concluded that productivity, morphological characteristics, and fiber fractions of B. decumbens (cv. Basilisk) were not affected by elevated atmospheric CO₂ in 30 months. These results are of great importance since B. decumbens is one of the main fodders in the Brazilian livestock production system, where extensive grazing is predominant and the herds depend almost exclusively on these grasses to meet their nutritional requirements. However, elevated CO₂ decreased forage Ca content, which can affect livestock production under a climate change scenario and needs further investigations.

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