Leaf Photosynthesis and Plant Competitive Success in a Mixed-grass Prairie: With Reference to Exotic Grasses Invasion

Table 1: List of C₃ species used in the photosynthesis-CO₂ response curve measurement.

The pots were overwintered by placing them in a shallow trench located on a sloping field on 8 Nov 2012. The tops of the pots were level with the soil surface, with soil around each tray of pots. They then were covered with an eight-inch thick layer of straw fastened down by a wire mesh. The pots were lifted on 5 May 2013, returned to the greenhouse and watered when needed. The photosynthesis survey of the major species was conducted from 11 Jun to 19 Jun 2013 under conditions similar to that for the A/Ci curve measurement survey in 2012. Leaf samples were collected on 25 June 2013 for total nitrogen content analysis. Also, specific leaf area was measured in order to convert leaf nitrogen content from the dry matter to leaf area basis.

Leaf photosynthetic rates measured under field conditions

Leaf photosynthetic rates for a wide range of plant species were measured on 13 days in 2008 (from 18 Jun to 18 Sep), 12 days in 2009 (1 Jun to 24 Sep) and eight days in 2010 (19 May to 21 Sep). The measurements were made within two 10 m×10 m exclosures located in one moderately grazed pasture and one extremely heavy grazing pasture. The vegetation within the exclosure was clipped to mimic the removal of herbage by cattle grazing. Photosynthesis measurements were made on clear or mostly clear days from 9 AM to 12 PM at a leaf temperature of 16.4 to 32.9ºC, PPFD of 500 to 1330 μmol m^-2 s^-1, and relative humidity of 28.3 to 65.5 percent. Measurements made on days when the volumetric soil water content at 23 cm depth of soil was lower than 0.2 (permanent wilting point in this prairie soil) are not included as we are interested in photosynthesis under less stressful conditions. During each of the three years, 16 to 20 plant species were measured in the exclosures (with each species measured four to 20 times). Grand averages of photosynthetic rates for each species under different grazing pressures were used in further analysis linking photosynthesis with leaf area index.

Leaf area index for individual plant species

A leaf area survey was conducted monthly four times during the growing season, May to September, for three years (2009 through 2011). A 1-m² frame was placed on two designated plots in the vicinity of the photosynthesis measurements. Four subplots within each frame were delineated and the percent contribution of total leaf area to the whole frame was noted for each. Separately, each subplot was visually surveyed to estimate leaf area by species. For each subplot, the value of each species’ contribution was adjusted to total 100 percent. The percent value of each species was then multiplied by the contribution of the subplot to the total frame. This information was combined with the total leaf area index within the 1-m² frame measured using a LP- 80 Ceptometer (Decagon Devices, Pullman, Wash. USA) to obtain the total leaf area of the frame by species.

Data analysis

The estimated eight parameters (Table 1) were subjected to principal component analysis (PCA) to identify the general trend of the multi-dimensional data sets. Differences in photosynthetic parameters among plant species were tested using one-way analysis of variance (ANOVA). As ‘photosynthetic capacity’ is often used to refer to maximum photosynthetic rates under no resource limitations, we denote the PCA-summarized variable as ‘photosynthetic potential.’ This is correlated with the long-term averaged frequency data for the 26 species. Also, grand averages of photosynthetic rates of dominant species were correlated with the corresponding leaf area indices estimated from field surveys from the same location. Data of leaf area index were square root transformed in order to meet the assumptions of the correlation analysis.

Results and Discussion

The first axis of PCA (Figure 1 - horizontal) is correlated with photosynthetic carboxylation (V_cmax) and electron transport (J_max) and the second (vertical axis) with the mesophyll conductance (G_meso) (Table 2). Six forbs (five from the Asteraceae family and one legume) had a greater intrinsic photosynthetic capacity than the remaining species, which occupied the middle or lower range of variation. Located at the lowest end of the horizontal axis were Poa pratensis, Bromus inermis and Taraxacum officinale F.H. Wigg. It appears that the maximum carboxylation rate (reflecting mainly the V_cmax in the first PCA axis) and the mesophyll conductance (the second PCA axis) may compensate to give similar maximum photosynthesis. In this respect, Achillea millefolium L. and Rosa arkansana Porter exhibited different patterns from other species (Figure 2). As shown in Figure 3, frequency was negatively correlated with photosynthetic potential of prairie plants, though the correlation was stronger when the information from the first two PCA axes were combined (Figure 3b, r=-0.435, p=0.026). Also, there was a positive correlation between photosynthetic rates and leaf nitrogen in these species (Figure 4). Furthermore, using our leaf photosynthesis data collected from 2008 through 2010 and leaf area index data for 25 species collected from 2009 through 2011, we observed also a negative correlation between leaf photosynthesis and plant success (here defined as leaf area within a unit land area) in both moderately and heavily grazed pastures, although the correlation was statistically weak (p=0.311 for moderate grazing and p=0.365 for heavy grazing), (Figures 5 and 6).

Figure 1: Principal component analysis (PCA) of seven parameters (V_cmax, J_max, R_dlight, G_meso, Γ*, Γ, and Anet) of the FvCB model based on the automated analysis scheme available at leafweb.ornl.gov. Abbreviations of plant species are defined in Table 1 and the abbreviations of parameters are defined in Table 2. The horizontal and vertical axes stand for the first and second axes of PCA, respectively, which account for 70 percent of the variance of the seven original parameters.

Figure 2: Relationships between maximum carboxylation limited photosynthesis (V_cmax) and mesophyll conductance (G_meso) (top panel) and electron transport limited photosynthesis (J_max) and mesophyll conductance (G_meso) (lower panel).

Figure 3: Correlation of plant frequency and photosynthetic potential defined as the first axis of the principal component analysis (PCA) of the seven photosynthetic parameters (a) and the combination of the first and second axes of the PCA analysis (b) for 26 C₃ plant species found in the mixed-grass prairie.

Figure 4: Relationship between photosynthetic rates and leaf nitrogen contents for prairie plants measured under common greenhouse conditions.

Figure 5: Correlation between photosynthetic rates and the square root of leaf area index of 16 plant species growing in a moderately grazed pasture. Photosynthetic rates were averaged based on measured values on 33 clear to mostly clear days during the growing seasons from 2008 to 2010, and leaf area indices were averaged values based on field surveys conducted in the same location from 2009 to 2011. Abbreviations of plant species are defined in Table 1, as well as: Psoarg=Pediomelum argophyllum (Pursh) J. Grimes [Psoralea argophylla Pursh] and Solmol=Solidago mollis Bartl.

Figure 6: The same as in Figure 5 except that the measurements were made on 20 species in a heavily grazed pasture. Abbreviations of plant species are defined in Table 1, as well as: Astagr = Astragalus agrestis Douglas ex G. Don., Lacobl =Lactuca tatarica (L.) C.A. Mey. var. pulchella (Pursh) Breitung [Lactuca oblongifolia Nutt.], Ratcol=Ratibida columnifera (Nutt.) Woot. & Standl., and Vicame=Vicia americana Muhl. ex Willd. et al.

Table 2: Correlation coefficients between the first three axes of the principal component analysis (PCA) and the seven photosynthetic parameters used in the PCA analysis. The analysis was based on the averaged data from photosynthesisintercellular CO2 concentration curves for 26 C3 rangeland plant species. Measurements were made at 28ºC, but the parameters were scaled to 25ºC. The percentages of variance of the original seven parameters explained by the PCA axes are included in the parentheses.

Averaged over the growing season from May to September, the leaf area indices of Poa pratensis and Bromus inermis combined accounted for 46 percent and 24 percent of the total LAI in plots of moderately and heavily grazed pastures, respectively (Tables 3 and 4). In terms of leaf nitrogen on ground area basis, the two exotic species combined represented 30 percent and 15 percent of the total leaf nitrogen of the plant communities under the two grazing treatments.

Table 3: Leaf area indices (LAI) and leaf nitrogen per unit ground area for 24 plant species found in a moderately grazed pasture in the mixed-grass prairie near Streeter N.D., USA.

Table 4: Leaf area indices (LAI) and leaf nitrogen per unit ground area for 38 plant species found in a heavily grazed pasture in the mixed-grass prairie near Streeter N.D., USA.

Past studies indicate that photosynthetic capacities of prairie forbs when compared to grasses are similar [20], higher [21] or lower [14,22]. Our results suggest that photosynthetic capacity of prairie forbs is widely variable, which is not surprising considering the number of plant families and life forms represented. The negative correlation between photosynthesis and plant frequency as observed in our study contrasts the findings of McAllister et al. [14] done in a highly productive tallgrass prairie. We speculate that the negative photosynthesis-plant success relationship as found in our study might indicate an outcome of severe interspecific competition for soil resources in the mixed-grass prairie.

The data from this study has several implications for understanding plant community and ecosystem functions in the mixed-grass prairie. First, the negative correlation between leaf photosynthesis and plant success suggests that the instantaneous photosynthetic characteristics measured at leaf level can only represent shortly-lived trends of leaf carbon gain, which cannot portray the overall photosynthetic capacity of the plant species during the entire growing season. Our measurements were conducted in the warm months, and did not capture photosynthetic activity in early spring and late fall when Poa pratensis and Bromus inermis maintain photosynthesis and growth while many other species in the prairie are dormant. Taking advantage of ample spring soil water for rapid growth is especially important for the competitive success of these two exotic species. Second, maintaining a low photosynthetic rate for the most abundant species also reduces excessive depletion of soil resources, and thus favors a more diverse plant community. This can also be seen from the peak-season value of the ground area-based nitrogen for each species co-occurring in the moderate and heavy grazing pastures (Tables 3 and 4). We can see that on a unit ground area basis on this prairie, these two exotic species are strong competitors for nitrogen, especially in the moderately grazed pasture. This occurred despite their low nitrogen content and low photosynthetic rate per unit leaf area.

Soil in this mixed-grass prairie typically is low in nitrogen (N) and phosphorus (P) and fertilization of N and P can increase forage production [23]. At the same time, high N application tends to favor exotic grasses such as Poa pratensis and reduce plant diversity, depending on stocking history [24]. Studies in the tallgrass prairie [25,26] also demonstrate that nitrogen addition may encourage native warm-season grasses to be displaced by exotic cool-season grasses such as Poa pratensis and Elymus repens (L.) Gould. It has been estimated that atmospheric nitrogen deposition due to burning of fossil fuels, crop fertilization and intensive livestock operations may increase plant N supply by 10-25 percent in the tallgrass prairie [27]. The relative contribution of nitrogen deposition may be higher in the mixed-grass prairie, perhaps as high as 50 percent, considering an estimated annual N mineralization rate of 1.2 g m^-2 [28] and an annual total atmospheric N deposition of 0.6 g m^-2 based on data of NADP for the year 2000. Bromus inermis and Poa pratensis, which are considered invasive [3] and investing larger proportion of its production to belowground biomass compared with co-occurring natives [29], have been shown to increase in both biomass production and cover on the silty range sites of the mixed-grass prairie over past 26 years, especially under rest and light grazing situations [15]. Wedin and Tilman [27] used a positive feedback model to describe the interaction between tallgrass prairie natives and soil nitrogen cycling. Perhaps the same framework can be used to speculate why in the mixed-grass prairie Poa pratensis and Bromus inermis have extensively displaced native grasses and forbs may partly be due to the low photosynthesis/low nitrogen, and low litter quality nature of these exotic species. Nevertheless, as the positive feedback system is inherently unstable, the future of the mixed-grass prairie will to a substantial extent be influenced by how the plant species, especially those representing a large fraction of LAI and per land area based nitrogen, such as Poa pratensis and Bromus inermis, allocate nitrogen among different organs and adjust their physiology strategies in response to various disturbances, including atmospheric N deposition at regional scale spanning tallgrass and mixed-grass prairies.

In addition to nitrogen deposition, other global change factors, such as increases in atmospheric CO₂ concentration and temperature, may have differential impacts to exotic vs. native species. A synthesis of available data suggests that invasive, noxious weeds have a larger than expected growth increase to both recent and projected atmospheric CO₂ increase as compared to native plant species [30]. Actually, it has been shown that, in Poa pratensis, increased atmospheric CO₂ concentration not only mitigated high temperature stress on net carbon gain, but also significantly increased root growth [31]. It will be interesting to test experimentally if this CO₂-related growth enhancement would increase the invasive potential of this and related species. Although our data showed a relative low photosynthetic potential in several invasive plants (Figure 1 and Table 2), the low mesophyll conductance measured in several invasive plants (Supplementary Table 1) suggests potentials for photosynthesis to increase under high atmospheric CO₂. To what extent this will be integrated into whole plant growth and competitive success is yet to be seen using manipulative experiments contrasting the invasive against the native plants, for which comprehensive data is merger yet critically important for understanding the integrity of rangeland ecosystems under future climate and land use changes [30]. As the invasion and naturalization of exotic plant species is influenced by not only biophysical but also social economic factors, including global trade [32], it will be a challenging task to constantly contain the vigor of the exotic species using a combination of tools, such as early grazing and prescribed fire targeted at the most vulnerable growth stages while maintaining the integrity of native species [4-6,33,34]. This highlights the importance of integrated, transdisciplinary studies for the rehabilitation of degraded rangelands [35].

Acknowledgements

This paper was part of North Dakota Agricultural Experiment Station projects ND6146, ND6147 and ND6149. We appreciate editors and reviewers for valuable suggestions that helped to improve the paper.

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