RESEARCH PAPER |
Photosynthetic properties of C4 plants growing in an African savanna/wetland mosaic
1Max Planck Institute for Biogeochemistry (MPI-BGC), Jena, Germany
2Nature Conservation and Plant Ecology Group, Wageningen University and Research Centre, The Netherlands
3Max Planck Institute for Meteorology, Hamburg, Germany
4Department of Physical Geography and Ecosystems Analysis, Lund University, Sölvegatan 12, 223 62, Lund, Sweden
5Harry Oppenheimer Okavango Research Centre (HOORC), Maun, Botswana
6Earth and Biosphere Institute, School of Geography, University of Leeds, Leeds LS2 9JT, UK
* To whom correspondence should be addressed at: Global Change & Biodiversity Programme, South African National Biodiversity Institute, Private Bag X7, Kirstenbosch Research Center, Cape Town, South Africa. E-mail: mantlana{at}sanbi.org
Received 4 March 2008; Revised 29 July 2008 Accepted 20 August 2008
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Abstract |
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Photosynthesis rates and photosynthesis–leaf nutrient relationships were analysed in nine tropical grass and sedge species growing in three different ecosystems: a rain-fed grassland, a seasonal floodplain, and a permanent swamp, located along a hydrological gradient in the Okavango Delta, Botswana. These investigations were conducted during the rainy season, at a time of the year when differences in growth conditions between the sites were relatively uniform. At the permanent swamp, the largest variations were found for area-based leaf nitrogen contents, from 20 mmol m–2 to 140 mmol m–2, nitrogen use efficiencies (NUE), from 0.2 mmol (C) mol–1 (N) s–1 to 2.0 mmol (C) mol–1 (N) s–1, and specific leaf areas (SLA), from 50 cm2 g–1 to 400 cm2 g–1. For the vegetation growing at the rain-fed grassland, the highest leaf gas exchange rates, high leaf nutrient levels, a low ratio of intercellular to ambient CO2 concentration, and high carboxylation efficiency were found. Taken together, these observations indicate a very efficient growth strategy that is required for survival and reproduction during the relatively brief period of water availability. The overall lowest values of light-saturated photosynthesis (Asat) were observed at the seasonal floodplain; around 25 µmol m–2 s–1 and 30 µmol m–2 s–1. To place these observations into the broader context of functional leaf trait analysis, relationships of photosynthesis rates, specific leaf area, and foliar nutrient levels were plotted, in the same way as was done for previously published ‘scaling relationships’ that are based largely on C3 plants, noting the differences in the analyses between this study and the previous study. The within- and across-species variation in both Asat and SLA appeared better predicted by foliar phosphorus content (dry mass or area basis) rather than by foliar nitrogen concentrations, possibly because the availability of phosphorus is even more critical than the availability of nitrogen in the studied relatively oligotrophic ecosystems.
Key words: C4 species, leaf nitrogen, leaf phosphorus, net photosynthesis, nitrogen use efficiency, specific leaf area, stomatal conductance
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Introduction |
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Plants of the C4 photosynthetic mode are capable of high photosynthetic rates at low intercellular CO2 concentrations (Hatch and Osmond, 1976), having high temperature optima (Long, 1985) and being highly efficient in assimilating carbon when exposed to full sunlight (Pearcy and Ehleringer, 1984; Piedade et al., 1991). It is now well established that C4 plants can attain high photosynthetic rates even under conditions of low resource (water and nitrogen) availabilities (Knapp and Medina, 1999), and they tend to dominate in hot environments characterized by seasonal soil water deficits (Hattersley, 1983; Collatz et al., 1998). Within the tropics, C4 grasses also dominate in permanent and seasonally waterlogged environments where tree maintenance and establishment is presumably not possible (Piedade et al., 1994; Long, 1999).
Due to the differing ecophysiological requirements of C3 and C4 plants, global climate change-related factors have the potential to shift the dynamic equilibria in ecosystems dominated by C3–C4 interactions (Ehleringer et al., 1997; Bond and Midgley, 2000). The major factors that constrain the relative abundances of C3 versus C4 species are water, nutrients, fire, and biotic stress. However, it remains difficult to quantify their overall contribution as the relative importance of each of these factors differs regionally (Sankaran et al., 2005). In the broadest terms, warmer growth conditions have been shown to favour C4 species over woody C3 species (Collatz et al., 1998; Sage et al., 1999). This difference has been attributed to the elimination of photorespiration by the C4 species, thus making their energy requirement for CO2 assimilation independent of temperature (Long, 1999). High atmospheric CO2 concentrations should improve the water status of both photosynthetic types through reduced stomatal conductance, but effects will be more marked for C3 types (Wand et al., 2001). Reduced ecological benefits in terms of water use efficiency (WUE) of C4 plants over C3 plants might, therefore, in grasslands, shift the probabilities of establishment towards C3 woody seedlings.
Nevertheless, surprisingly little is known about the short-term and small-scale response to environmental factors of C4 species growing across a range of natural ecosystems, even within a single region. Such data may be useful for the validation of processes in models that simulate land surface fluxes (Collatz et al., 1992; von Caemmerer and Furbank, 1999). Since the seasonality of water and nutrient availability are the two major factors that constrain C4 gas exchange (Knapp and Medina, 1999), gas exchange, leaf nitrogen, and leaf phosphorus content of C4 species growing in natural environments that differ in their long-term water availability, ranging from permanent swamp to rain-fed grassland, were characterized. The chief objective was to determine whether the dominant species that grow in these very different habitats would, under non-limiting soil water conditions at the time of measurement, differ in terms of their leaf photosynthetic capacity, as estimated by the light and CO2 response curves, and how photosynthetic capacity changes with leaf N and leaf P. These data were used to determine if there were systematic effects of long-term hydrological regime on the photosynthetic traits of the characteristic C4 species found at a particular location.
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Materials and methods |
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Study area
Three study sites of different hydrology within the Okavango River Delta, Botswana were selected. The Okavango River flows from the Angolan highlands into Botswana where it spreads into a complex, dynamically changing mosaic of perennial swamps, seasonal swamps, floodplains, and rain-fed grasslands and savannas. The herbaceous types of vegetation which dominate much of the Delta are dominated by C4 grasses and sedges, but also contain a number of C3 species, especially in the moister areas (Ellery et al., 1992).
Although the rainy season in the southern part of Africa typically lasts from November to March, the Delta is sustained by rainfall collected in its Angolan catchment, which usually reaches its upper parts (dominated by permanent swamps) shortly after the rainy season ceases, around April or May, then reaching its distal parts (dominated by seasonally flooded grasslands, dry grasslands, and savannas) around July or August when the dry season is near its peak. The level and area of surface flooding vary distinctly between the northern and the southern parts, as well as on a micro-scale within any area of >1 km2 or so.
In the perennial swamps, some of the typical plant communities are formed by Cyperus papyrus and Phragmites australis, together with Miscanthus junceus, Typha latifolia, and Imperata cylindrica as co-dominants. One of the study areas was chosen in the central region of these perennial swamps, close to the Jao distributary channel (S19° 01.18' E22° 24.03'). In this area, peat has gradually accumulated, indicating a prevalence of inundated conditions.
The second study area (S19° 36.06' E23° 16.07') represented a typical seasonal floodplain with the sedges Schoenoplectus coryombosus and Cyperus articulatus growing in its lowest parts. The clay, representing the predominant soil material here, becomes blackish in colour when wet. Panicum repens dominated slightly higher areas with less seasonal inundation, and I. cylindrica was found on the upper, drier areas of the floodplain (Mantlana et al., 2008). Panicum repens and I. cylindrica were found in areas that have soils with a sandy-loam character.
The third area investigated was a rain-fed grassland (S19° 39.06' E23° 21.53'), located in an area that had not received flooding for several years, and possibly for decades. Here, the top 30 cm of the soil consisted predominantly of sand. The vegetation was dominated by annual and perennial grasses, Urochloa trichopus, Cynodon dactylon, and Eragrostis lehmanniana, together with a forb, Pechuel loechea. Around the edge of the study area, there were trees of the genera Lonchocarpus, Acacia, and Phoenix. An overview of the species measured in this study and some relevant characteristics are found in Table 1.
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Gas exchange measurements
Measurements were carried out during the second half of the rainy season undertaken in February and March 2003 (Table 2), providing the opportunity to study plant gas exchange of the various species present in the different areas under close to optimum soil moisture conditions and to investigate whether clear differences emerge that are related to the different growth conditions at the sites. Steady-state leaf gas exchange measurements were made using an open gas exchange system (LI-6400; Li-Cor Inc., Lincoln, NE, USA). Within each study area, at least 4–5 individuals of the dominant species were selected at random for measurements on fully expanded leaves. Measurements were made between 0900 h and 1600 h and were recorded only after photosynthetic rate and stomatal conductance were considered constant and at equilibrium with the ambient conditions within the gas exchange cuvette. For each measured leaf, light-saturated photosynthetic rate, Asat, stomatal conductance, gsat, and the ratio of internal to ambient CO2 concentration, Ci/Ca, were first obtained as averages of three measurements at high photon irradiance (1600, 1800, and 2000 µmol m–2 s–1) and at an ambient [CO2] of 380 µmol mol–1. Subsequently A:Ci response curves were determined at high photon irradiance (>1600 µmol m–2 s–1) and at different chamber [CO2] in the sequence ambient, 300, 200, 100, 50, ambient, 600, 800, and 1000 µmol mol–1. For every leaf sampled, light and CO2 response curves were fitted individually by a non-linear regression (SPSS 12.0 for Windows) to the hyperbolic function, y = a (1 – eb–cx), (Causton and Dale, 1990) where y is the rate of CO2 exchange, x is the independent variable (I or Ci), and b and c determine the slope of the curve and were allowed to vary for each curve-fitting procedure. In the case of light response curves, coefficient a gives the light-saturated rate of CO2 exchange (Asat), b/c gives the compensation point, a(1 – eb) gives the dark respiration, and the apparent quantum yield (the slope, or derivative of the curve at the light compensation point) is given by aceb. In the case of the A:Ci curve, a represents the light- and CO2-saturated rate of CO2 exchange (Apot), the CO2 compensation point,
, is again calculated from b/c, and the carboxylation efficiency (the slope, or the derivative of the curve at the CO2 compensation point) is given by aceb (for all, see Causton and Dale, 1990; Midgley et al., 1999). This simple equation has been widely used to analyse light and CO2 response curves of a variety of species (Midgley et al., 1999; Wand et al., 2001; Kgope, 2004) and fitted the data well (r2 
0.9; Table 3). Gas exchange characteristics of C. papyrus were determined from its umbel section, since it is the most productive part of the plant (Jones, 1988). Gas phase limitation to photosynthesis, Lg, was estimated from [(Apot – Asat)/Apot] (Farquhar and Sharkey, 1982; Long, 1985).
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After completion of the gas exchange measurements, the leaves were scanned and their area calculated afterwards using WinFOLIA software (Regents Instruments Inc., Quebec, Canada). Leaf dry weight was obtained after oven-drying at 70 °C for 24 h, and C and N concentration were measured using a Vario EL (Elementar Americas, Inc., Mt Laurel, NJ, USA; Mantlana et al., 2008). Specific leaf area (SLA) was determined as the ratio of the measured leaf surface area divided by leaf dry weight. Leaf phosphorus concentration was measured after a nitric acid digestion using ICP-AES (atomic emission spectrometry with inductively coupled plasma; Perkin-Elmer, Norwalk, CT, USA; Mantlana et al., 2008). Nitrogen use efficiencies (NUEs) were determined by dividing Asat by leaf N, and are expressed on a leaf area basis. Bivariate relationships between foliar N and P concentrations (both dry weight and area basis), Asat, and SLA were evaluated using standardized major axis (SMA) regression (Warton et al., 2006) using the program SMATR (Falster et al., 2006). SMA regression is a regression method preferred when one is more interested in the true slope of a relationship, rather than predicting values for a dependent variable from a predictor variable. It is thus commonly used to establish allometric scaling relationships, especially when the two variables are not measured on comparable scales (Warton et al. 2006).
Meteorological and soil variables
At the seasonal floodplain, half-hourly rainfall, air temperature, and air water vapour saturation deficit at 
3 m height were measured at a nearby eddy-covariance flux tower, using a tipping bucket rain gauge (Young; Model 52202, R. M. Young Company, Traverse City, MI, USA), temperature probe (HMP45A, Vaisala, Helsinki, Finland), and RPT 410 Barometric Sensor (Druck, New Fairfield, CT, USA), respectively. At the perennial swamp and the semi-arid rain-fed grassland similar meteorological data, at 7 m and 3 m height, respectively, were collected at a nearby mobile tower using equipment similar to that used in the seasonal floodplain. Volumetric soil water content (
) was measured at each microhabitat within the floodplain, at 0–5, 5–10, and 10–15 cm soil depth intervals using a battery-powered hand-held soil moisture sensor (Moisture Meter type HH2 with Theta probe, Delta T Devices, Cambridge, UK) during each measurement campaign.
For each site, 12 – 15 soil samples were collected at intervals of 0– 5, 5–10, 10–20, and 20–30 cm. These were then air dried (sandy soils from the rain-fed grassland) or oven dried at 40 °C (loam, clay, and peat soils from seasonal floodplains and perennial swamp, respectively) before being analysed for carbon and nitrogen using Vario MAX (Elementar Americas, Inc.). Soil nutrient data reported here are for the upper 10 cm of soil.
To test the significance of differences among the species in leaf traits and gas exchange parameters, data were analysed with univariate analysis of variance (ANOVA), using Tukey's HSD test or the t-test. Statistical analyses were performed using the SPSS (SPSS 12.0 for Windows) statistical package.
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Results |
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Environmental conditions during measurements
Daily mean maximum air temperatures (Ta) during the study period were similar across the three habitats, ranging from 33 °C to 35 °C (Table 2). Nevertheless, mean vapour pressure deficit (D) at the rain-fed grassland exceeded those at the permanent swamp by
0.7 kPa. The measurement periods at the rain-fed grassland and, to a lesser extent, the seasonal floodplain were associated with unusually high rainfall events. In one case, >200 mm of rain fell in 1 d. Still, mean volumetric soil water content () at 10 cm soil depth was lowest at the rain-fed grassland (0.18 m3 m–3) and highest at the permanent swamp (0.42 m3 m–3) with the seasonally flooded grassland intermediate (0.30 m3 m–3), reflecting the different soil physical properties. Soil C:N, at 0–10 cm depth, showed no significant difference between the sites (ANOVA, n=52, F=2.75, P=0.74) and was 13.9 at the swamp, 14.9 at the seasonal floodplain, and 11.8 at the rain-fed grassland (Table 2).
The different environmental conditions encountered during measurements were also reflected in the leaf chamber conditions. Leaf temperatures (Tl) at the rain-fed grassland and seasonally flooded grassland were typically 38 °C, slightly higher than at the permanent swamp (35 °C) (Table 4). Similarly, mean leaf-to-air vapour pressure deficit (Dl) was between 4 kPa and 5.3 kPa at the two grass-dominated sites, while those at the permanent swamp were significantly lower (ANOVA, n=60, F=23.9, P <0.01) at 3.7 kPa (Table 4). These differences in microclimate were unavoidable as the three sites were sufficiently far from each other to preclude any measurement strategy covering all sites on just 1 d. There were also other logistical (e.g. vehicular) constraints on the measurement strategies possible. However, it is thought that the observed differences were small enough not to affect the results or conclusions presented below more than just marginally.
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Gas exchange parameters at ambient conditions
Photosynthetic rates and maximum stomatal conductances differed significantly, both between species at a given site and across sites. The species growing at the permanent swamp displayed the largest within-site differences, with mean Asat of M. junceus, 52 µmol m–2 s–1, being almost twice that of the proximally growing C. papyrus, 27 µmol m–2 s–1 (Fig. 1). Interspecific variations at the seasonal floodplain were smaller, with Asat ranging from 25 µmol m–2 s–1 to 31 µmol m–2 s–1. Significant differences at this site (ANOVA, n=19, F=4.19, P=0.03) in Asat were found between I. cylindrica and C. articulatus only. At the rain-fed grassland, the annual grass, U. trichopus, had the highest mean Asat, 47 µmol m–2 s–1, which was significantly higher (ANOVA, n=19, F=5.17, P=0.018) than that of the co-existing perennial grass, C. dactylon (36 µmol m–2 s–1), only.
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At all three sites, there were also significant differences in mean gsat between species. At the permanent swamp the observed pattern was similar to the one for Asat: M. junceus had the highest mean value, 0.32 mol m–2 s–1, and C. papyrus had the lowest, 0.22 mol m–2 s–1 (Fig. 1). Despite Asat varying little for the three species examined for the seasonal floodplain, mean gsat of the sedge, C. articulatus, 0.23 mol m–2 s–1, was
25% greater than that of the two perennial grass species growing close by. At the rain-fed grassland, gsat was within the same range as that at the seasonal floodplain (0.2–0.3 mol m–2 s–1), and values were similar among the perennial grasses (0.21 mol m–2 s–1), but these values were significantly lower (ANOVA, n=19, F=6.88, P <0.05) than those found in the annual grass, U. trichopus. Mean chamber Dl during the measurement period (Table 4) did not vary at a given site, with the exception of data collected for U. trichopus where Dl was significantly lower (ANOVA, n=19, F=15.55, P <0.01) than for the other two species. The ratio of intercellular to ambient CO2, Ci/Ca, reflects the changes in the relationship between stomatal conductance and rate of net CO2 assimilation. Light-saturated ratios at the permanent swamp differed significantly (t-test, t=7.8, n=16, P <0.01) between the highest values (C. papyrus, 0.41), and lowest values in M. junceus, 0.22 (Fig. 1). This range in Ci/Ca was similar to that observed at the seasonal floodplain where mean Ci/Ca of the sedge C. articulatus, 0.4, was almost 2-fold higher than that found in the co-existing P. repens (0.16) and almost twice that of I. cylindrica (0.24). Among the species at the rain-fed grassland, mean Ci/Ca values were lower when compared with the other sites, and showed no significant difference (ANOVA, n=19, F=1.8, P=0.19) despite varying by a factor of two on average (0.10–0.19).
A:Ci response curves
CO2 response curves of all the species yielded very low CO2 compensation points (; Table 5), which were similar for the species growing at the permanent swamp and in the seasonal floodplain (8–11 µmol mol–1) and three times as high as those observed for the species growing in the rain-fed grassland (3–6 µmol mol–1; Table 5). The species at the latter site also had the steepest initial slope of CO2 response curves (
), ranging on average from 3.2 µmol m–2 s–1 (µmol/mol)–1 to 3.6 µmol m–2 s–1 (µmol/mol–1), indicating the highest efficiency of CO2 utilization at low Ci (Table 5). These values exceeded those of the species at the permanent swamp and the seasonal floodplain by a factor of 4–6, where average ranged from 0.5 µmol m–2 s–1 (µmol/mol)–1 to 1.6 µmol m–2 s–1 (µmol/mol)–1. Overall Ci at the rain-fed grassland site did not exceed 300 µmol mol–1, even at high chamber Ca, of 800–1000 µmol mol–1 (Fig. 2), whereas Ci at the floodplain and the permanent swamp were 400 µmol mol–1 at high Ca.
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The range in average net photosynthesis rates at saturating light and CO2 concentration, Apot, at the permanent swamp and at the rain-fed grassland was nearly identical, ranging from 38 µmol m–2 s–1 to 56 µmol m–2 s–1, while species from the seasonal floodplain had overall lower Apot,
34–39 µmol m–2 s–1 (Table 5). Short-term increases of chamber CO2 concentration above ambient levels led to increased photosynthetic rates in all species, as indicated by the estimation of gas phase limitation to photosynthesis, Lg. The higher the Lg of a particular species, the further its Asat operates from Apot (Long, 1985). Perennial grasses at both the permanent swamp and the seasonal floodplain were within the same range of Lg, 8–17%, and lower than the co-existing sedge species, 27%. Despite tending to operate at a lower Ci/Ca, the species at the rain-fed grassland showed the weakest response to a short-term increase of CO2 as indicated by the low range of mean Lg of 5–10%, but overall there was no statistical difference (ANOVA, n=12, F=0.71, P=0.52) at this site.
Net CO2 assimilation rates in relation to foliar nitrogen and phosphorus concentrations
Figure 3a shows the relationship between Asat and leaf nitrogen expressed on a leaf area basis (Na), the latter of which varied considerably across the study, from 16 mmol m–2 to 166 mmol m–2. Variation in Na between species for the plants growing in the permanent swamp was large and highly significant (ANOVA, n=18, F=251.6, P <0.01), and this was also reflected in the large variation in NUE which was much smaller in the sedge (0.26 mmol mol–1 s–1 on average) than in the co-existing grasses, M. junceus and I. cylindrica (0.94 mmol mol–1 s–1 and 1.64 mmol mol–1 s–1, respectively; Fig. 4). Leaves of all plants sampled on the seasonal floodplain had relatively low Na (43–78 mmol m–2), and NUE varying from 0.46 mmol mol–1 s–1 to 0.78 mmol mol–1 s–1 (Fig. 4). These values were only slightly lower than those determined at the rain-fed grassland site (Na, 52–120 mmol m–2; NUE, 0.49–0.65 mmol mol–1 s–1). In contrast, Na showed no significant differences among the co-existing species for either the rain-fed grassland (ANOVA, n=16, F=2.68, P=0.11) or the seasonal floodplain (ANOVA, n=17, F=1.69, P=0.22).
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Figure 3a suggests that within a given species there is a positive relationship between Asat and Na (and in a similar way Apot; not shown). However, across all species investigated, the overall relationship was poor and not significant (r2=0.02; P=0.45; SMA regression).
Variations in Asat were, however, closely related to variations in foliar phosphorus when expressed on a leaf area basis (Pa), not just within a given species, but also across species within a given site and between sites (r2=0.24; P=0.002; SMA regression; Fig. 3b). Nevertheless, as observed for Na, it was also the case that M. junceus and I. cylindrica at the permanent swamp had higher Asat at any given Pa than the other species examined. The large variation in Asat at the permanent swamp (Fig. 1) would therefore seem to be well accounted for on the basis of variations in Pa, and the generally lower Asat for the seasonally flooded grassland, especially in comparison with the rain-fed grassland (Fig. 1), also appears accountable in terms of the significantly higher (t-test, t=13.8, n=25, P <0.01) Pa of the latter.
The general C3 plant scaling relationships for Asat versus Na and Pa as given by Wright et al. (2004), also based on using SMA regression, are shown as dashed lines in Fig. 3a and b. In both cases the present data show a drastically different response, with all C4 species having a much sharper response than is typically observed for C3 plants. Photosynthetic rates at a given Na or Pa were 5- to 10-fold higher than would be predicted from the generalized relationship given by Wright et al. (2004). Note, however, that the present analyses were made using replicates of species, while those of Wright et al., (2004) were established on species means. It should also be noted that the present results merge intraspecific, interspecific, and intersite variation. While the present data point to a possibly different response of C4 plants, it is clear, also when considering the variability between the C4 species encountered in this study, that a larger number of samples from a wider range of C4 environments is required to ascertain this observation.
General aspects of the ‘leaf economic spectrum’
Figure 5 illustrates pairwise relationships between foliar properties, allowing a more general evaluation of leaf property differences among the species studied here and comparing the relationships found with established relationships previously established by Wright et al. (2004). Independent of being expressed on an area or dry weight basis, phosphorus emerges as a better predictor of Asat than nitrogen (r2=0.66 versus r2=0.23). Observed values of Asat at any given foliar N or P concentration were much higher in the current study than would be predicted from the relationships established by Wright et al. (2004). However, the general relationship between foliar N and P on a dry weight basis (Fig. 5c) was similar to the one postulated by Wright et al. (2004).
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Figure 5d and e shows the relationship between SLA and leaf N and P (again on a dry weight basis). In both cases, the C4 grasses investigated here had significantly higher SLA than would be expected for C3 plants characterized by similar foliar N or P concentrations. As for Asat, phosphorus proved to be a markedly better predictor of SLA than did nitrogen (r2 of 0.51 and 0.18, respectively; SMA regression with SLA–1 as the y variable as in Wright et al., 2004).
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Discussion |
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Leaf-level photosynthetic rates at light saturation,
25–50 µmol m–2 s–1, were comparable with those obtained for other C4 tropical plants growing in their natural environment under optimum light, water, and nutrient conditions (30–50 µmol m–2 s–1; Long, 1985; Baruch, 1996). Similarly, the range of gsat observed in this study, 0.15–0.32 mol m–2 s–1, was well within that of C4 species under optimum growth conditions, i.e. 0.2–0.4 mol m–2 s–1 (Lawlor, 2001). Under saturating light and low Dl, leaves of C4 plants commonly show a range of Ci/Ca from 0.25 to 0.4 (Lawlor, 2001). High Ci/Ca values of 0.41–0.45 as found for the two sedge species in this study may be typical for tropical C4 species that dominate wet habitats (Jones, 1988; Piedade et al., 1994). This suggests that a low Ci/Ca among C4 tropical species growing in their natural habitat is not necessarily a universal phenomenon (Grace et al., 1998). Still, the low gsat taken together with low Ci/Ca in the grasses of the rain-fed grassland and the seasonal floodplain suggest that these species would retain significantly higher daily WUE than their co-existing sedge species, or grasses growing in the permanent swamp. The relatively non-conservative WUE of sedges versus grasses is probably retained throughout most of the year, as was the case at the seasonal floodplain (Mantlana et al., 2008). The ecological benefit for higher WUE in this semi-arid environment would be the lengthening of the daily period of carbon acquisition and growth, as it maintains high CO2 assimilation at reduced water loss.
The low compensation points found in this study are typical of C4 plants (Lawlor, 2001). At the rain-fed grassland in particular, the markedly high indicates a very efficient re-fixation of photorespiratory CO2 by phosphoenol pyruvare carboxylase (PEP-C), as has been observed in laboratory studies (von Caemmerer and Furbank, 1999). In addition, the high found at the rain-fed grassland implies that species in this site had either more efficient PEP-C or higher levels of the enzyme when compared with species from the other two habitats (von Caemmerer, 2000). Previous studies have mentioned that in C4 plants maximal PEP-C activity affects primarily the initial slope of the CO2 response curves (Polley et al., 1992; Pfeffer and Peisker, 1998; Shenton et al., 2006). These results may be a reflection of the slightly higher leaf N found in this habitat, as PEP-C content is positively related to leaf N (von Caemmerer, 2000) while nitrogen deficiency decreases both Rubisco amount and activity, and also carboxylation efficiency in C4 plants (Long et al. 1985; von Caemmerer, 2000). In a similar way as discussed for the Ci/Ca, the results suggest that under well-watered field conditions, C4 species from different natural habitats differ significantly in their efficiency of CO2 utilization at low Ci, with species from the dry habitats showing higher efficiency than those from the wet habitats.
The grasses were operating closer to Apot than co-existing sedge species, as indicated by their lower gas phase limitation to photosynthesis, Lg. Relatively higher Ci/Ca in the sedges, as discussed above, was thus associated with relatively higher Lg, suggesting that factors other than CO2 demand in the stomata were responsible for the observed high Lg.
Previous field studies have also reported high values of NUE in C4 species (Baruch et al., 1985; Anten et al., 1998; Simioni et al., 2004). Given the high NUE of C4 plants, it is therefore not surprising that the photosynthesis scaling relationship observed for the C4 species in this study showed a significantly greater slope than in the ‘general’ C3 case. Since the higher NUE of C4 plants is generally associated with a more efficient use of Rubisco, this suggests that under natural conditions these plants would have an ecological advantage in situations of nitrogen limitation (Long, 1999), for instance by allocating more carbon to tissues involved in acquisition of the resources that are most limiting to plant growth (Sage et al., 1987).
Although high Apot among the grasses at the permanent swamp can be explained by the combination of a fast turnover rate of Rubisco giving rise to a high NUE as is commonly found amongst NADP species (Ghannoum et al., 2005), overall photosynthetic rates were best correlated with leaf P contents, which, along with N, may play a central role in the regulation of the photosynthetic carbon reduction (PCR) cycle (von Caemmerer, 2000). Phosphorus supply is potentially limiting in 30% of terrestrial ecosystems, including boreal forests, tropical forests, and savannas (von Uexkull and Mutert, 1995). The phosphorus supply rate directly affects CO2 fixation (Jacob and Lawlor, 1991; Campbell and Sage, 2006) as was demonstrated by a decrease in photosynthesis in phosphate-deficient leaves of sunflower, maize, and wheat plants (Jacob and Lawlor, 1991). At forest sites in Hawaii, addition of P increased above-ground productivity at P-limited sites more strongly than at N-limited sites, although foliar P concentration was similar at both sites (Harrington et al., 2001), and at a rainforest in Cameroon leaf gas exchange responded somewhat more strongly to phosphorous than to nitrogen, although the difference was small (Meir et al., 2007).
For savannas, interspecific differences have been observed in the nutritional requirement of C4 grasses from different ecological regions, with nitrogen requirements for production of organic matter generally increased by addition of phosphorus (Bilbao and Medina, 1990). One explanation for the generally low foliar P levels of the plants growing in the seasonal floodplain is a reduced availability of phosphorus under aerobic soil conditions when the plants are actively growing, for example due to the precipitation of ferrous phosphate [vivianite, Fe3(PO4)2·8H2O] (Zachara et al., 1998). It is also likely that overall low rates of mineralization under anaerobic conditions in both the seasonally and permanently flooded grasslands may have resulted in increasingly large amounts of soil P being bound in less plant-accessible forms (Chacón et al., 2005). Thus, while an increasing amount of data from tropical species suggest an equally strong, perhaps stronger effect of phosphorus on gas exchange or growth, the exact mechanism is not yet clear.
The present data set is limited by using replicates of a small number of species, but the overall range encountered in the data is comparable with the GLOPnet data set used in Wright et al. (2004). For instance, the latter included a log LMA=1.2–3.2, log Nmass= –0.6 to 0.8, and log Pmass= –0.2 to –2.1, whereas the present data covered log LMA=1.4–3.3, log Nmass= –0.3 to 0.5, and log Pmass= –0.5 to –1.5. The observed leaf N versus SLA relationships showed the pattern typically observed in relation to leaf economy (Wright et al., 2004): long-lived leaves tend to have low Nmass at low SLA, a pattern that was also observed for the perennial species in this study. The opposite is found for short-lived leaves and, accordingly, the highest SLA and highest foliar N concentration were observed in the annual grass Urochloa. Across the two locations where Imperata was measured, its SLA and Asat varied widely, while consistently having relatively low foliar N levels. This adaptable leaf economy of Imperata may be one of the reasons for its success as an invasive species under many environmental conditions.
The well known relationship between foliar nitrogen contents (dry weight basis) and SLA are attributed to accommodate for higher photosynthesis rates (area basis) at given Na if foliar N (DW) contents are high (Reich et al., 1999). It is therefore interesting that in the current study foliar P seems to correlates somewhat better with SLA than does foliar N. The reasons for this are unclear, but, as for photosynthesis, it does suggest that phosphorus, as opposed to nitrogen, was the most critical element modulating variations in plant ecophysiological characteristics of the species studied here. A study comparing a cultivated African grass species with a South American pasture grass showed that the African species was more dependent on P supply than on N supply, for maximal growth (Bilbao and Medina, 1990). These results suggest that there may be a differentiation among the studied wetland savanna C4 species according to their P and N requirements for growth and their capability to exploit soil nutrient sources. Moreover, the general tendency for lower soil fertility to be negatively correlated with levels of dominance of C4 grasses over C3 trees and shrubs in savanna ecosystems (e.g. Goodland and Pollard, 1973; Lopes and Cox, 1977) may at least be partly explainable in terms of the much lower photosynthetic nutrient use efficiencies of the latter.
In conclusion, the present results showed that since species at the rain-fed grassland experience high D even during the height of the rainy season that may lead to high transpiration rates, they possess strategies (low Ci/Ca and high leaf N) that allow them to reduce water loss and achieve light-saturated photosynthesis close to their potential rates that are at least as high as those of permanent swamp and seasonal floodplain species. However, the gas exchange behaviour that was observed would occur only during periods of adequate soil water content for plant growth. The data do not imply that throughout the year the grasses from the rain-fed grassland would fix similar rates of CO2 per unit loss of water compared with species from the permanent swamp and seasonal floodplain. In fact, the above-ground living biomass is greatly reduced during the dry months, and the overall efficient physiology during the rainy season reflects an optimum use of resources during a short active season. Moreover, the cost of the water conservation strategy of the grasses at the rain-fed grassland was apparent in their lower NUE compared with grasses from the permanent swamp. The results suggest that leaf P plays an important role in determining the ecological performance of C4 tropical grasses, perhaps through modulating the degree to which these grasses respond to nitrogen acquisition. Because of their role in supporting carbon assimilation in plants, understanding the metabolic demand for leaf N and leaf P is crucial in improving our knowledge of C4 plant growth in natural ecosystems.
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Acknowledgements |
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This research was funded by a grant from the Deutsche Forschungsgemeinschaft to AA. EMV was supported through University of Botswana Research funds; KBM acknowledges support from MPI-BGC and from Wageningen University scholarships. We thank Ines Hilke for leaf nutrient analyses and Michael Schwarz, Nadine Hempel, Thebe Kemodisele, Billy Mogojwa, and Ineelo Mosie for their invaluable field assistance. We also thank Harry Oppenheimer Okavango Research Centre and Department of Water Affairs in Gumare for providing logistical support during the field campaigns. Two anonymous reviewers provided helpful criticism to improve the manuscript considerably.
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Abbreviations |
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A, net photosynthesis;
, carboxylation efficiency; Apot, potential net photosynthetic rate; Asat, light-saturated photosynthetic rate; Ci/Ca, ratio of intercellular to ambient CO2 concentration; D, vapour pressure deficit; Dl, leaf-to-air vapour pressure deficit; gs, stomatal conductance; gsat, light-saturated stomatal conductance; Lg, gas phase limitation to photosynthesis; NUE, photosynthetic nitrogen use efficiency; PEP-C, phosphoenol pyruvare carboxylase; PCR, photosynthetic carbon reduction cycle; Rubisco, ribulose bisphosphate carboxylase oxygenase; SMA, standardized major axis; , soil water content; Ta, air temperature; Tl, leaf temperature; WUE, water use efficiency; , CO2 compensation point. |
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