PHOTOSYNTHESIS OF INDIAN WOODOATS IN CENTRAL TEXAS WOODLANDS

Texas has been divided into ten major plant zones (Correll & Johnston 1979). These “zones” are not plant communities and have been called vegetation regions or biomes, which is not correct (Van Auken 2018). They are physiographic regions described by physical geography or geomorphology. Hill (1892) first called Central Texas the Edwards Plateau and the name has been widely adopted (Gould 1975a; 1975b; Correll & Johnston 1979; Amos & Gehlbach 1988; Van Auken 2018). Some have suggested this is too simple an approach and have divided the area into four smaller but more specific areas that are not plant community types either (LBJ School of Public Affairs 1978; Riskind & Diamond 1988). More recently, the ecological regions of Texas, and more specifically the vegetation of Texas, has been mapped (Elliott et al. 2014), however, there are many plants, especially those with lower densities that are not well delineated.

Plants in woodlands or forests, similar to those in central Texas, can be separated vertically into overstory, understory and plants in-between. In addition, there is horizontal separation, those growing in the open high light and those growing below a canopy in low light as well as those growing at the edge. Species present below closed forest or woodland canopies generally have photosynthetic rates that are low compared to species in the open (Zangerl & Bazzaz 1983; Hättenschwiler & Körner 1996; Hirose & Bazzaz 1998; Hull 2002). If true understory plants are exposed to high light levels more characteristic of open grassland communities or disturbed habitats, gas exchange rates do not generally increase very much (Larcher 2003; Keddy 2017). Edge or intermediate plants can increase carbon fixation dramatically (Boardman 1977; Larcher 2003; Keddy 2017). Many species in central Texas savannas have responses to light levels that have been difficult to predict, possibly because of recent community changes including encroachment or habitat manipulation.

In central and eastern Texas, as well as much of southeastern North America Chasmanthium latifolium (Michy.) Yates (Indian woodoats or woodland oats, Poaceae/Gramineae), a grass species, is found below woodland or forest canopies (USDA NCRS 2021). Sometimes this species is found in uplands but more commonly in riparian forest washes, creeks, streams and on rivers banks (Brown & Smith 1974). This species is morphologically very similar to Uniola paniculata L. (Figure 1). Early on, both species were placed in the genus Uniola (Holm 1891a; 1891b). In 1966 the nine species of Uniola, which seemed to separate into two habitat types, were placed into three genera, Chasmanthium (five species), Uniola (two species) and Leptochloöpsis (two species) (Yates 1966a; 1966b; 1966c).

The two habitat types were (1) the wet woodlands and forests of southeastern North America and (2) the dry coastal habitats of eastern North America, Central America and northwestern South America. The Chasmanthium species in the relatively wet or damp forest or woodland habitats were in low light understories. Three of the species of Uniola and Leptochloöpsis were costal sand dunes species growing in high light. The western limits of the Chasmanthium species in Texas were below the woodland and riparian forest canopies in central Texas (USDA NCRS 2021). However, Chasmanthium latifolium does occur very sporadically in New Mexico and Arizona in some riparian communities, but the other Chasmanthium species are farther east.

The species in these two habitats seem to be different photosynthetic types based on leaf anatomy (Yates 1966a; 1966b; 1966c) and ¹³C/¹²C ratios (Smith & Brown 1973). These characteristics for Uniola and Leptochloöpsis suggest the C₄ photosynthetic pathway. For the Chasmanthium species the characteristics suggest the C₃ photosynthetic pathway (Smith & Brown 1973; Cerling et al. 1997; Ehleringer & Sandquist 2015; Keddy 2017). Plants with C₄ photosynthesis have high rates of carbon fixation at high light levels (full sun) while plants with C₃ photosynthesis usually have lower rates of carbon fixation at high light levels (Boardman 1977; Larcher 2003; Keddy 2017; Poorter et al. 2019). In addition, C₃ plants usually have a positive carbon fixation rate at low light levels, higher than that of C₄ plants (Wayne & Van Auken 2009; 2011). There is usually some overlap at the high and low light levels depending on the species and other factors can influence carbon fixation rates including temperature, CO₂ level, humidity, soil water and soil nutrient levels (Boardman 1977; Larcher 2003; Keddy 2017; Poorter et al. 2019).

Uniola paniculata (sea oats) has high rates of photosynthesis like other C₄ species (Valero-Aracama et al. 2006) and a number of conservation and reclamation studies have been completed with this and related species (Gormally & Donovan 2011; Gormally et al. 2013). However, the same is not true for the C₃ understory Chasmanthium species. Chasmanthium latifolium is found in low light riparian woodlands and forests in eastern and central Texas (Gould 1975a; 1975b; Correll & Johnston 1979; USDA NCRS 2021). I have not identified any studies of the photosynthetic rates of any of the species of Chasmanthium in Texas or elsewhere.

The present study examined the light response of leaves of Chasmanthium latifolium in the understory of a Juniperus ashei/Quercus fusiformis (Ashe juniper/live oak) canopy. Gas exchange rates were measured to decide if its understory presence is related to its gas exchange or photosynthetic properties.

Site description.—Plants studied were below a Juniperus ashei/Quercus fusiformis canopy on private property (98.681W, - 29.698 N) approximately 48 km north of San Antonio, Texas, near the southern edge of the Edwards Plateau just north of the Balcones Escarpment. Soils were Crawford Series, stony clay, shallow over hard limestone, zero to three percent slope, non-calcareous clay about 20–22 cm thick with limestone below (Mollisol over limestone bedrock, USDA NRCS 2017).

Annual mean temperature was 20°C with monthly means from 9.6°–29.4°C (1981–2020, NOAA 2020). Precipitation was 78.7 cm/yr, bimodal, with peaks in May and September (10.7 cm and 8.7 cm, respectively, 1981–2020, NOAA 2020), with little summer rain, high evaporation and high variability.

Area vegetation was Juniperus-Quercus savanna or woodland, but higher in woody plant density than communities farther west (Van Auken et al. 1979; Van Auken et al. 1980; Van Auken et al. 1981; Smeins & Merrill 1988). Woody species were Juniperus ashei (Ashe juniper) and Quercus fusiformis (plateau live oak), Diospyros texana (Texas persimmon) and Dermatophyllum secundiflorum (Texas mountain laurel). Chasmanthium latifolium was present at low density usually in areas that were not grazed (USDA NCRS 2021).

Interspersed in the woodlands were sparsely vegetated inter-canopy patches or gaps (Van Auken 2000). Herbaceous vegetation below the canopy was mostly Carex planostachys (cedar sedge, Wayne & Van Auken 2008). The gap species included Aristida longiseta (red threeawn), Bouteloua curtipendula (side-oats grama), Bothriochloa laguroides ssp. torreyana (silver bluestem), B. ischaemum var. songarica (King Ranch bluestem), various other C₄ grasses, and a variety of herbaceous annuals (Correll & Johnston 1979; Enquist 1987). Light levels and soil temperatures were higher in the gaps than the associated woodland (Wayne & Van Auken 2004; Boeck & Van Auken 2017).

Gas exchange.—A Li-Cor 6400 portable photosynthetic meter was used to measure gas exchange and light levels. Photosynthetic-flux density (PFD) was the fixed variable. Plants were fully leafed out in April 2020 when leaves were measured (± three h of solar noon). Gas flow was 400 μmol/s and the CO₂ concentration was 400 μmol/mol with PFDs as follows: 0, 5, 10, 25, 50, 75, 100, 200, 400, 600, 800, 1000, 1200, 1600, 1800 and 2000 μmol/m²/s. Measurements were started at the highest light level then recorded after two-three minutes when the coefficient or variation stabilized at < 1%, at which point the PDF was reduced to 1800 and measurements continued through the sequence indicated above. Three separate leaves from adjacent plants (20–30 cm above the soil surface) were placed next to each other across the narrow width of the chamber so they covered the entire surface of the chamber. This represented one of five replicates measured (Van Auken et al. 2020). Temperature and relatively humidity were set at 16^oC and 34 % respectively.

Fully expanded leaves on plants below a Juniperus ashei/Quercus fusiformis canopy were measured on a clear, cloudless day (April 16, 2020). Understory light level was 203 ± 28 μmol/m²/s (mean ± SE) and range was 29 to 335 μmol/m²/s. Light levels at or above the canopy were 1897 ± 21 μmol/m²/s.

Calculated or measured gas exchange values were as follows: maximum photosynthetic rate (A_max = μmol CO₂/m²/s), photosynthetic-flux density PFD at A_max (μmol/m²/s), transpiration at A_max (μmol H₂O/m²/s), conductance at A_max (mmol H₂O/m²/s), light saturation point (μmol/m²/s), dark respiration (μmol CO₂/m²/s), light compensation point (μmol/m²/s), and the quantum yield efficiency (μmol CO₂/μmol quanta). Data for each replicate measurement was fit to the model of Prioul & Chartier (1977) using the PC software package Photosyn Assistant (Dundee Scientific, Dundee, Scotland).

A_max was the highest net photosynthetic rate. Light saturating photosynthesis was the PFD when the slope of the initial rate line reached the A_max. Dark respiration was the gas exchange rate at a PFD of 0 μmol/m²/s (y-intercept of the line for the initial rate). The light compensation point was the PFD when the photosynthetic rate was 0 μmol CO₂/m²/s (x-intercept of the line for the initial rate). The quantum yield efficiency was the dark value and increasing PFDs until the regression coefficient decreased.

Light response curves were generated for each replicate. Assumptions for parametric statistics were met (Shapiro Wilk test for normal distribution and Bartlett test for equal variance (Sall et al. 2007)). A one-way ANOVA was completed for the variables followed by the Tukey Kramer HSD to determine if differences occurred at various PFD levels (Sall et al. 2007). An alpha value of 0.05 was used.

Presented first is a photosynthetic light response curve for Chasmanthium latifolium growing in the understory of a Juniperus ashei/Quercus fusiformis canopy in central Texas at a light level of 203 ± 28 μmol/m²/s (mean ± SE) (Figure 2). Results appear to be a polynomial function with a high R² value (0.997). Mean photosynthetic rates reached a plateau as light levels increased. Each black dot is the mean of five replications. The p value for the one-way ANOVA was <0.0001. The mean photosynthetic rate for the leaves of C. latifolium was 5.48 ± 1.30 μmol CO₂/m²/s ranging from −0.34 to 12.92 μmol CO₂/m²/s over the 16 light levels measured. Negative values at lower light levels indicate respiration was greater than CO₂ uptake. Significant differences in photosynthetic rates (Tukey Kramer HSD, p<0.05) were detected between several of the light levels but there was considerable overlap between measurements (Figure 2). Light levels with the same letter (above or below the mean) are not significantly different (Tukey Kramer HSD, p>0.05). There were no significant differences between light levels of 1200 and 2000 μmol/m²/s nor between 0 and 100 (Figure 2). Care has to be used to see difference among other light levels because of data overlap. It should be noted that photosynthetic levels were positive but low even at 5 μmol/m²/s.

Both transpiration and conductance were measured as a function of light level and are shown sequentially (Figures 3 and 4). These rates were measured at the same time photosynthetic rates were measures on the same replicates. Plot results are best represented by polynomial functions with high R² values (>0.95). ANOVA results were very highly significant for both transpiration and conductance rates (p<0.0001) Transpiration rates decreased from a mean high of 2.266 μmol H₂O/m²/s at the highest light level to 0.652 μmol H₂O/m²/s at a light level of 75 μmol/m²/s. From there the transpiration rate increased as the light level approached zero with no significant differences in values. There were no significant differences in transpiration rates between 2000 and 1200 μmol/m²/s or between 0 and 600, but they were some significant differences between 600 and 1200 μmol/m²/s (Tukey-Kramer HST, p < 0.0001). Mean stomatal conductance followed a similar trend but water loss is much lower (Figures 3 and 4). Values indicated stomates were open and functioning.

The mean maximum photosynthetic rate (A_max) for leaves of C. latifolium was estimated at 13.92 ± 0.50 μmol CO₂/m²/s (Table 1). The quantum yield efficiency or initial slope (ϕ or IS) for leaves of C. latifolium was 0.013 ± 0.001 μmol CO₂/μmol quanta (Table 1). The light compensation point (L_cp) was 6 ± 2 μmol/m²/s, the light saturation point (L_sp) was 1027 ± 42 μmol /m²/s and dark respiration (R_d) was 0.08 ± 0.09 μmol CO₂/m²/s (Table 1). Stomatal conductance at the A_max was 0.155 ± 0.017 and the transpiration rate at the A_maxwas 2.266 ± 0.042 (Table 1).

point (L_sp) was 1027 ± 42 μmol /m²/s and dark respiration (R_d) was 0.08 ± 0.09 μmol CO₂/m²/s (Table 1). Stomatal conductance at the A_max was 0.034 ± 0.017 and the transpiration rate at the A_maxwas 2.265 ± 0.042 (Table 1).

When the A_max rate of Chasmanthium latifolium was compared with the A_max of a C₄ grass such as Bouteloua curtipendula from a high light habitat, the C₄ grass had an A_max rate 2.3 times higher than C. latifolium (Wayne & Van Auken 2011) (Figure 5). When photosynthesis was compared at low light levels (shade, 100 μmol/m²/s) values of the two species were very similar, but at 10 μmol/m²/s photosynthetic rates for C. latifolium were low but positive (Figure 5). For B. curtipendula carbon uptake at this light level was negative, that is, only respiration was occurring. While CO₂ uptake for C. latifolium was low, it was still positive.

The A_max of C. latifolium was 2.8 times higher than that of Carex planostachys, a known woodland understory species (Table 1). An open habitat member of the borage family (Heliotropium tenellum) had an A_max rate 2.5 times higher than C. latifolium (Table 1). Six facultative species had intermediate photosynthetic rates and were thought to be canopy edge species (Furuya & Van Auken 2009; Gagliardia & Van Auken 2009; Furuya & Van Auken 2010; Van Auken & Bush 2011). Photosynthetic rates of these species were modified by the light levels they were exposed to, but usually had A_max values less than the C₄ grasses. The A_max of C. latifolium was lower or approximately equal to the A_max of these species. Populations of C. latifolium have been noted in various mixed central Texas riparian woodlands usually along intermittent creeks. The environments where this species has been observed are low light environments below the canopy of riparian woodlands in Central Texas and not in open grasslands.

Interestingly, gas exchange rates for C. latifolium at higher light levels were within the range of other intermediate photosynthetic species including most C₃ species (Boardman 1977; Larcher 2003; Begon et al. 2006). Other photosynthetic parameters, including light saturation, light compensation, dark respiration, conductance, and transpiration, were within the range of values for many C₃ species (Table 1). These responses are consistent with findings for some shade plants, but closer to values reported for facultative species (Boardman 1977; Hull 2002; Larcher 2003; Givnish et al. 2004; Valladares & Niinemets 2008; Van Auken & Bush 2015). The parameters measured for shade adapted leaves of C. latifolium at elevated light levels increased but suggested that C. latifolium can grow in the understory and is more of an intermediates light level species capable of growth in low to medium light environments. Also suggested is that it will not usually be found in high light environments such as open grasslands. No C. latifolium plants were found in full sun, consequently we do not know if they could acclimate to a variable light environment as seen for example in light gaps such as reported for other species (Hull 2002; Valladares & Niinemets 2008).

Respiration rate of leaves of C. latifolium growing in shade below a Juniperus ashei/Quercus fusiformis canopy was estimated at 0.08 ± 0.09 μmolCO₂/m²/s or about 12% of values for other species growing in similar habitats (Hirose & Bazzaz 1998; Hull 2002; Van Auken & Bush 2015). Dark respiration for shade-adapted species is normally low due to lower metabolic rates (Bjorkman 1968; Bazzaz & Carlson 1982). Respiration of Polygonum pensylvanicum, a wetland plant grown in low light, was about 0.5 μmol·CO₂/m²/s, whereas the rate for its leaves in full sun was twice as high (Bazzaz & Carlson 1982). Grunstra & Van Auken (2015) measured dark respiration at various temperatures for other species in this area and did not find significant differences. Other gas exchange values reported for C. latifolium are within the range or lower than values reported for similar intermediate light requiring or edge adapted species.

Where a species is found is determined by conditions present in that habitat and the response of the species to those conditions. However, unraveling the specific characteristics and levels of the factors present is challenging (Smith & Smith 2015; Keddy 2017). I believe that C. latifolium usually grows in shade, and gas exchange characteristics indicate that is its habitat preference which is where the C₄ grasses cannot grow because of higher light requirements (Wayne & Van Auken 2011). However, photo-inhibition of leaf pigments or overheating of leaves (Begon et al. 2006) or shallow roots (Johnson et al. 2018) could be problematic and comparable patterns of distribution of other species were caused by differential herbivory (Louda & Rodman 1996; Maron & Crone 2006; Leonard & Van Auken 2013). As a personal observation, C. latifolium is occasionally used in some high light plantings where it seems to do well, however, if high light competitors are present it will likely be overgrown and replaced.

Dr. Clark Terrell was very helpful locating Chasmanthium latifolium plants. Mr. Hector Escobar showed me how to use the LiCor 6400 photosynthetic meter. Dr. Janis K. Bush made supplies available for the LiCor 6400. Mr. Jason Gagliardi showed me how to use JMP statistical programs. Mr. Charles Wu of the UTSA Library found some obscure literature that was very helpful. Ms. Genna Calkins-Mushrush and Ms. Laurie Yarger of the West Custer County Library were very helpful with some new computer and remote internet issues.