Resilience of warm-season (C4) perennial grasses under challenging environmental and management conditions

Abstract

Warm-season (C4) perennial grasses are the main source of nutrients for livestock in tropical and subtropical regions with warmer temperatures. Climate change and increasing global temperatures may favor the expansion of areas with C4 grasses, previously occupied by C3 plants. Although C4 grasses are known for their resilience under stressful defoliation management, differences in anatomical and morphological characteristics can affect the resilience of these species to management practices. In addition, N is usually the most limiting nutrient for C4 grasses, while growing and the combi nation of N supply along with defoliation intensity and frequency may dictate the expansion and perennation of different C4 grass species in newly populated areas. In addition to greater forage production, C4 grasses have potential to increase CO2 mitigation due to the efficient photosynthetic pathway. A greater proportion of the biomass accumulation in C4 grasses occurs below ground, increasing C concentration in the soil and potential C sequestration. In summary, the expansion of C4 grasses in the world due to climate change has potential to increase forage production for livestock and mitigate greenhouse gas emissions in agriculture systems. Warm-season (C4) perennial grasses are widely spread and dominant in tropical and subtropical regions, between 30oN and 30oS latitude, and it is perceived that more than two-thirds of all grasses in these regions are C4. The most extensive natural C4 biomes are the various savannas of the tropics, subtropics, and warm temperate areas that range in C4 grass cover from 20% to nearly pure C4 grassland (Cole, 1986; Figure 1). However, C4 grasses are spread in temperate regions and can be important forage resources for livestock during the growing season in those locations (Moser et al. 2004). According to Sage et al. (1999), at warm-temperate latitudes, C4 species dominate grassland productivity, even though they may represent less than 60% of the grass flora of the region. It is estimated that C4-dominated grasslands support approximately 40% of the world’s ruminant animals (Moser et al. 2004) and it is an important source of nutrients and shelter to several wildlife species in Africa, South America, North America, and Oceania (Sanderson et al., 2004). Cow-calf pair grazing ‘Mislevy’ bermudagrass [Cynodon dactylon (L.) Pers.] in Florida. Temperature has been the most significant factor dictating the presence or persistence of C4 grasses in a specific location and growing season. Temperature is highly correlated with C4 abundance along both latitude and elevation gradients. According to Long (1983), C4 plants are not dominant where growing season temperatures are less than an average of 16 °C and minimum mid-summer temperature average less than 8 °C. Increasing atmospheric temperatures (global warming) may favor the dominance of C4 species in different ecosystems, therefore, management practices may have to be adjusted accordingly. Cerling et al. (1997) observed that stable carbon isotopic data collected over the past 20 years document a worldwide expansion of C4 grasslands through the displacement of C3 vegetation during the Late Miocene and Pliocene. Corroborating with those findings, Wang et al. (2015) observed that increasing temperatures caused a shift from C3 to C4 species in the desert steppe in China, as indicated by the decrease in C3/C4 ratio due to warming temperatures over a 6-yr period. The expansion of C4 grasses in these areas may be detrimental to biodiversity, but it may not be avoidable due to the decline of the native vegetation and aggressive propagation mechanisms of C4 grasses. The C4 carbon fixation pathway, identified by Hatch and Slack (1966) is responsible for the adaptability of warm-season grasses in locations with high temperatures worldwide. The environmental regions with predominantly C4 grasses range from wetlands to deserts and some of the least productive to the most productive ecosystems on the earth (Wedin, 2004). It was later observed that C4 species had different decarboxylation systems and were divided into three main groups based on differences in the activities of C4 decarboxilation enzymes, named NAD-Malic (Hatch and Kagawa, 1974), NADP-Malic (Berry et al., 1970), and PEP carboxykinase (PCK, Edwards et al., 1971). The three groups all have similar leaf cell anatomy; however, there are some structural variations, which appear to correlate with biochemical differences and may potentially impact the regions of adaptability of the main groups. Dominant tall C4 grasses from different species are adapted to different regions of the world, such as big bluestem (Sorghastrum nutans L.) in North America, kangaroograss (Themeda australis (R.Br.) Stapf.) in northern Australia, thatchingrass (Hyparrhenia spp.) in South Africa, and bluestem (Andropogon spp.) in Brazil, which tend to be malate forming (NADP-Malic) enzyme variants. These locations are characterized by relatively high humidity and these grasses are usually managed at low-input levels (Vogel et al., 1978; Wedin et al., 2004). Taub (2000) compared the C4 grass flora and climatic records for 32 sites in the USA and found that the proportion of the grass flora that uses the NADP-Malic enzyme variant of C4 photosynthesis greatly increases with increasing annual precipitation, while the proportion using the NAD-Malic enzyme variant and PCK decreases. The NAD-Malic and PCK usually have greater growth potential and nutrient requirement, while the NADP-Malic group has slower growth rates, with greater cell wall deposition and efficient N use. Taub (2000) observed that there was a strong correlation between the frequency of the different subfamilies with annual precipitation that was independent of the influence of the different C4 variants. It therefore appears that other, as yet unidentified, characteristics that differ among grass subfamilies may be responsible for their differences in distribution across natural precipitation gradients and the association of grass subfamilies with annual precipitation was even stronger than for the C4 decarboxylation variants. Besides the importance of the climatic conditions to different groups, soil fertility, and management conditions may interfere with the adaptability of C4 grasses with different enzyme variants to a specific location. Plant N use efficiency (NUE) has been a variable of interest, primarily in extensive grazing systems with low N inputs. The NUE may be due to variations in the efficiency of the photosynthetic apparatus, such as enzyme kinetics. In general, it is expected that NADP-Malic plants have low late season forage N concentration (<5.0 g/kg), while aspartate forming (NAD-Malic and PCK) plants usually have greater tissue N concentrations (10–20 g/kg) (Wedin, 2004). LeCain and Morgan (1998) found that leaf N concentration was higher in three NAD-Malic grass species than in three NADP-Malic grasses, implying that NAD-Malic species may compensate for a lower NUE with greater allocation of N to photosynthetic organs. Bowman (1991) compared four NAD-Malic and two NADP-Malic members of the grass genus Panicum and found that at high levels of N availability the NAD-Malic species had higher shoot N concentrations than the NADP-Malic species. The NADP-Malic species may have a greater photosynthesis rate than NAD-Malic species at a given leaf N concentration. However, this trial compared subtypes within the same species and there may be larger inter-species variations. The NAD-Malic plants may have relatively greater N requirement than NADP-Malic, primarily due to greater enzymatic steps and amino acids (Kanai and Edwards, 1999). Superior NUE of NADP-Malic relative to NAD-Malic grasses is achieved with less leaf N, soluble protein, and Rubisco having a faster turnover (Ghannoum et al., 2005). Lambers and Poorter (1992) hypothesized that low potential growth rates are associated with species found in N-poor habitats. Recently, there has been identified genes related to NUE in crops. Genes that code for nitrate and ammonium transporters that assimilate N from the soil and genes that synthesize N compounds such as glutamine synthetase, which produces the amino acid glutamine (used to transport N through the plant) are examples of genes that have been recently evaluated to increase NUE in crops (Hirel at al., 2007). The identification and expression of these genes may be of great interest to forage crops, which are commonly cultivated under a limited supply of N fertilization; however, these preliminary studies have been conducted only in major crops, such as maize, rice, and wheat. Native and planted grasslands are frequently found in soils with limited production capability, many times in highly weathered, acid, and less fertile soils. Soil microorganisms, pH, structure, texture, organic matter, water, and many other characteristics influence forage growth, however, soil fertility is one of the most influential characteristics in forage production. The combination of low soil nutrient levels, efficient nutrient extraction capability, and high total yield potential create conditions for significant yield responses when grasslands are fertilized (Matthews et al., 2004). Nitrogen is the most limiting plant nutrient for growth of grasses and yield and increasing crude protein (CP) responses have been observed with different species (Wilkinson and Langdale, 1974). Nitrogen has the greatest influence on forage yield and accordingly influences the amount of other nutrients required to sustain production at specific N levels (Taliaferro et al., 2004). Nitrogen is essential for amino acids and protein synthesis and formation of nucleic acids, which increase photosynthesis and forage production. The increase in DM production is frequently justified by the increase in tiller numbers, tiller weight, number of leaves per tiller, and leaf appearance rate in warm-season grasses (Moreira et al. 2009; Premazzi et al., 2003; Colozza et al., 2000). Premazzi et al. (2003) observed an increase in tiller number and weight on ‘Tifton 85’ bermudagrass (Cynodon spp.) fertilized from 0 to 160 mg N/kg and there was a significant correlation between tiller number and DM accumulation. Moreover, N fertilization also increases the number of leaves per tiller and leaf appearance rate. Garcez Neto et al. (2002) observed a quadratic increase in tiller number, leaf appearance, and leaf elongation rate of ‘Aruana’ guineagrass (Panicum maximum Jacq.). Leaf appearance rate ranged from 0 to 0.14 leaves/d and leaf elongation from 25 to 60 mm/d with N fertilization levels from 0 to 200 mg/dm3. Santos et al. (2009) observed that leaf elongation rate increased from 15.4 to 46.8 mm/d in ‘Marandu’ palisadegrass [Brachiaria brizantha (Hochst.) ex A. Rich] with N fertilization levels of 0 and 100 kg/ha, respectively. It has been observed that N fertilization may not increase root-rhizome mass in warm-season forages (Alderman et al., 2011); however, it may affect carbohydrate reserve utilization. Nitrogen fertilization has decreased root-rhizome carbohydrate concentration of bermudagrass (Schmidt and Blaser, 1969). Root-rhizome mass and carbohydrate concentration are important factors involved in C4 grass regrowth and persistence; therefore, a combination of fertilization and adequate levels of defoliation frequency and intensity should be imposed to promote persistence of C4 grasslands. Liu et al (2011) observed that taller stubble heights promoted greater total nonstructural carbohydrate mass in Tifton 85 bermudagrass pastures grazed from 8 to 24 cm stubble height. It is perceived that N fertilization may be a source of nutrient contaminant to waterways due to leaching and off-site movement; however, most C4 grasslands are managed extensively without or limited amounts of N fertilization, primarily due to economic constraints (Vendramini et al., 2014). In addition, C4 grasses efficiently uptake N and are used for phytoremediation of soils with increased nutrient concentration (Newman et al., 2009) and soil cover to decrease erosion and run-off (Sanderson et al., 2004). Defoliation is a major determinant in C4 grassland productivity and persistence and it can be caused by fire, pests, mechanical harvest, or grazing. The resilience of the C4 grasses to defoliation is attributed to a combination of morphological and physiological characteristics. Newly expanded grass leaves in the upper canopy are the primary site of photosynthesis, and as grass leaves age, they senesce and become less efficient in the use of solar energy for plant growth (Pitman, 1994). The upper leaves are usually the first tissues removed when the grassland is subjected to grazing, therefore decreasing primary production. Severe defoliation may remove photosynthetically active leaves, partially or completely, and carbohydrates stored in the reserve organs become the main substrate for energy for regrowth. It is observed that the most commonly used C4 grasses in subtropical areas have the ability to allocate photosynthate between reserve structures (rhizomes, stolons, and roots), and store C and N that can be remobilized after grazing, which are crucial for rapid regrowth after severe defoliation (Moore et al. 2004). If the defoliation is lenient, the plant will restore leaf area and photosynthesis will become the main supplier of energy. It is also noted that the most resilient grasses under grazing have meristematic zones positioned at, or below the soil surface, and they are therefore inaccessible to grazing animals. Additionally, the meristematic region is located at the base of the leaf, thus new leaf material can continue to grow even if older parts of the leaf are removed by grazing (Chapman and Lemaire, 1993). In addition to the robust reserve structures and protected meristematic points, some C4 grasses have avoidance mechanisms, which reduce the probability of defoliation of the plant by grazing animals. Those mechanisms can be morphological, such as stem elongation, thorns, etc. or antiquality chemical components. According to Richard (1993), the degree of stress imposed depends on defoliation depends on frequency and intensity of defoliation, physiological age and type of removed tissue, and the occurrence of stress or competition before, during, or after the defoliation. There has been an extensive investigation on management practices to quantify optimum dynamics of leaf area expansion, light capture, and sward structural and compositional changes in C4 grasses (da Silva et al. 2015); however, research demonstrating persistence and productivity of C4 grasses under a stressful defoliation regime is scarce. This information is valuable because a great proportion of C4 grasses are cultivated under marginal management practices. In general, new cultivars were selected and released over the last 50 years with the main objective to increase herbage accumulation and nutritive value, and this selection may have altered plant morphology, physiology, and preference by animals, which may negatively impact persistence. Vendramini et al. (2010) conducted a grazing trial to test the effects of different grazing frequencies on newly released cultivars of bahiagrass (“Tifton 9” and UF Riata) under a limited N fertilization regime. It was observed that Tifton 9 and UF Riata bahiagrass cultivars decreased root-rhizome mass and ground cover when grazed at 2 wk when compared to a 4 wk regrowth interval; however, Tifton 9 had greater root-rhizome mass than Argentine, Pensacola, and UF Riata when grazed at a 4 wk regrowth interval. It is recommended that new cultivars should be tested under a range of management practices, thus clear management guidelines are defined upon the release of the cultivar. Stocking rate is the most common animal-based measure of grazing intensity and it is suggested that it is more important than any other single grazing management decision (Jones and Jones, 1997; Sollenberger et al. 2012). The main objective of numerous grazing intensity studies during the past five decades was to describe the form of the performance per animal curve as a function of stocking rate or grazing pressure (Sollenberger and Newman, 2007). Burns et al. (1989) compiled a series of grazing studies with fixed stocking rates and observed that average daily gain (ADG) is predominantly greater at low stocking rates. In low stocking rates, the animals have the option to ad libitum consumption of selected leaf components, which maximizes ADG. Increasing stocking rates may increase gain per hectare up to a limit where additional increase would result in limiting herbage mass and consequently reduction in ADG and gain per hectare (Mott and Lucas, 1952). Although C4 grasses are known for their resilience under stressful defoliation management, few studies in the literature have reported the deleterious effects of grazing intensity and stocking rates on C4 grasses’ persistence. Rouquette et al. (2011) reported the effects of stocking rate on persistence of “Coastal” or common bermudagrass pastures with different fertilization and cool-season annual forage management and concluded that stands of Coastal and common bermudagrass were negatively affected by greater stocking rates and lack of N fertilization. Bahiagrass was the primary nonbermudagrass invasive species, while Coastal bermudagrass pastures grazed at greater stocking rates had a greater incidence of invasive bermudagrass ecotypes. et al. observed that bermudagrass pastures grazed at high stocking rates with average stubble of 9 cm decreased stands from to and increased invasive common bermudagrass from to Stocking is a defined or to animals in and to a specific objective et al., Stocking are usually defined into two main or The effects of stocking on resilience of C4 grasses have not been in research Sollenberger et al. conducted a literature and evaluated that or stocking an increase in forage for According to greater herbage accumulation occurs because the stocking livestock distribution by increasing livestock and in grazing which the It is hypothesized that stocking of stubble and regrowth interval. grazing intensity is a crucial of C4 grassland the of grazing may not impact plant as as the stubble is at the optimum levels for the specific C4 species. Sollenberger et al. concluded that to and grazing the of grazing season of grazing, and or any other grazing will not be to this and animal responses to stocking rates and are species and management specific and should be not among different production therefore, a to grassland should be identified for a grazing stored in grazing to of world’s soil C et al., and increase of of in the cm of grazing soils is to the total agriculture emissions The C4 grasses have potential to increase CO2 mitigation due to the efficient photosynthetic and biomass accumulation. In addition, a greater proportion of the biomass accumulation in C4 grasses occurs below ground, increasing C concentration in the soil et al., The C4 grasslands of the global but have of the global soil organic C and 2000). It has been observed that common management practices used to increase forage nutritive value, and persistence can increase soil C and in grasslands et al. et al. found that bahiagrass pastures fertilized with N had greater soil C than bahiagrass with N fertilization and in Florida. the increase in C it is perceived that N fertilization may increase which would the of greater soil C accumulation. However, many C4 grass grazing have extensive grazing systems with or fertilization. et al. observed that there was in emissions in bahiagrass fertilized with limited N fertilization levels and with N of the emissions in grasslands are from N while are from animal et al., In of the potential greater C C4 grasses have usually greater cell wall and concentration than C3 plants et al., which may increase production in the However, several management practices can be used to decrease emissions by C4 grasses, such as of in the and use of such as and among et al., and et al., In summary, the in global temperatures the expansion of C4 grasses in regions previously occupied by C3 plants. 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