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Ecology |
2Wetland Biogeochemistry Institute, Department of Oceanography and Coastal Sciences, Louisiana State University, Baton Rouge, Louisiana 70803 USA; 3Plant Biology, Department of Biological Sciences, Aarhus University, Ole Worms Alle Building 135, 8000 Aarhus C, Denmark; 4South Florida Water Management District, 3301 Gun Club Road, West Palm Beach, Florida 33416-4680 USA
Received for publication January 3, 2005. Accepted for publication June 14, 2005.
ABSTRACT
Phosphorus (P) availability limits plant growth in many ecosystems. The ability of plants to explore for soil P is often impaired by nonresource stressors. Understanding the effects of these stressors on P acquisition in oligotrophic environments is critical in predicting species dominance. Growth and nutrient responses of Eleocharis cellulosa to redox intensity and phosphate level were evaluated under three redox potentials (Eh) and three phosphate (PO4) levels (P). Although low Eh (–150 mV) decreased root length at low P, Eh did not affect shoot height, relative growth rate (RGR), shoot elongation, photosynthesis, or biomass of E. cellulosa. Low PO4 (10 µg P · L–1) strongly inhibited growth. Shoot height, RGR, elongation, photosynthesis, and biomass were lower at 10 µg P · L–1 than at 80 or 500 µg P · L–1. None of the growth variables, except the ratio of root-supported biomass to root biomass, significantly differed between the 80 and 500 µg P · L–1 treatments. At low P, plants allocated relatively more biomass to roots than to shoots, compared to the medium and high P levels. Eleocharis cellulosa is well adapted to flooded conditions that lower soil Eh, and elevated PO4 levels further promote its growth potential.
Key Words: biomass • Cladium jamaicense • Eleocharis cellulosa • Everglades • flood adaptation • nutrient accumulation • nutrient use efficiency • photosynthesis
Phosphorus is an essential macronutrient for plant growth. However, P often becomes a limiting factor in many ecosystems (Shaver and Melillo, 1984
; Vitousek, 1984
; Fourquerean et al., 1992
). Especially in calcareous soil systems, such as seagrass ecosystems in Florida Bay (Fourquerean et al., 1992
), mangrove islands in the Caribbean (Feller et al., 1999
), and herbaceous wetlands in Central America (Rejmánková, 2001
), P is relatively unavailable due to precipitation with calcium carbonate. One important mechanism by which plants adapt to a low P availability is by increasing their ability to acquire P (Raghotama, 1999
). Although plant responses, including enhanced P uptake kinetics, production of cluster roots, and increased root phosphatase activity, can increase P acquisition, a common response in many plants such as rice is to enhance root absorption area by increasing root length (Kirk and Du, 1997
). Phosphorus is relatively immobile in soils, and hence a laterally extensive and deep root system is essential for maximizing soil exploration and P utilization. However, the ability of roots to explore soil P is often impaired by nonresource stressors such as soil anoxia (Rubio et al., 1997
). An understanding of the effects of nonresource stressors on the ability of plants to acquire nutrients in oligotrophic environments is critical in predicting species dominance and thus is a necessary requirement for the wise management of these ecosystems.
The oligotrophic Florida Everglades is one such environment where P limits plant growth (Craft and Richardson, 1995
, 1997
) and plant success is dependent upon the ability of the plants to successfully acquire P by root exploitation of the soil. Much of the Everglades is characterized by peat soil with various amounts of marl overlying a limestone base of recent marine origin (Loveless, 1959
). Everglades peat is rich in calcium carbonate and thus possesses a high capacity for P precipitation as Ca-P-minerals (Koch and Reddy, 1992
; Richardson and Vaithiyanathan, 1995
). Therefore, dissolved reactive phosphate in undisturbed Everglades is extremely low, 2–14 µg · L–1 (Koch and Reddy, 1992
). The natural Everglades has been greatly impacted by anthropogenic activities. Phosphorus levels in the northern Everglades has increased due to runoff from adjacent agricultural areas (Richardson et al., 1999
) and has altered the vegetative communities of the Everglades, an oligotrophic wetland ecosystem (Urban et al., 1993
; Davis, 1994
). One apparent habitat change has been the disappearance of thousand hectares of wet prairie/slough community in some areas (Loveless, 1959
; Ogden, 2003
).
In addition to increased P input to the Everglades, the natural hydrology of the Everglades has been dramatically altered by water management practices during the last century (Walters, 1992
; Fennema et al., 1994
; Light and Dineen, 1994
). Resultant changes in hydroperiod and water level can differentially affect oxygen entry into the soil, creating a variable redox environment and the potential for root oxygen deficiencies. Root elongation requires oxygen at the root meristem. Hence, soil flooding is one of primary environmental constraints for wetland plants (Mendelssohn and Burdick, 1988
; Pezeshki, 2001
), a constraint that can influence P acquisition. Soil flooding or hydrological alteration strongly influences soil oxidation–potential (Eh) (Gambrell and Patrick, 1978
), a response observed in the Everglades. Low soil Eh of –100 to –200 mV, due to prolonged soil flooding, is common in the Florida Everglades (Qualls et al., 2001
). Thus, root oxygen deficiencies, as a result of this high redox intensity, may be another important factor limiting the growth of plants in the Everglades (Chabbi et al., 2000
). The periodically flooded conditions in the Everglades require plants adapted to a changing redox environment.
Due to the combined effects of nutrient enrichment and altered hydroperiod, the vegetative community of the Everglades has undergone dramatic changes (Davis et al., 1994
). From the 1960s to the 1980s, the mean percentage cover of wet prairie and slough communities significantly decreased from 48% to 35%, while sawgrass-dominated communities significantly increased from 39% to 50% (Davis et al., 1994
). Specific wet prairie/slough species like Eleocharis cellulosa Torr. have decreased in dominance in some areas (Loveless, 1959
; Ogden, 2003
). In contrast, the Cladium jamaicense (Crantz) community in certain regions has expanded into areas previously occupied by wet prairie communities (Davies et al., 1994
). However, little experimental evidence is available concerning what might be causing these changes in wet prairie/slough communities (Edwards et al., 2003
; Busch et al., 2004
; Daoust and Childers, 2004
). Because increased P input and altered hydrology are the two dominant environmental changes that have co-occurred in the Everglades, we assessed their effects on E. cellulosa, a dominant wet prairie/slough species.
The specific objective of this study was to quantify the effects of redox intensity and phosphate level on root and shoot growth, photosynthesis, biomass allocation, and nutrient content of E. cellulosa, using a controlled Eh-hydroponic system (Lissner et al., 2003a
, b
). We hypothesized that low Eh, simulating a prolonged flooding stress, would induce a reduction in growth, root length, and nutrient uptake of E. cellulosa across a broad range of phosphate levels. In this study, we investigated the growth response of E. cellulosa to three redox intensities (–150 mV [strongly reduced], +150 mV [moderately reduced] and +600 mV [oxidized]) and three phosphate levels (10, 80, and 500 µg P · L–1) during a 2-month experimental period. This is the first study of this species' response to P availability under controlled redox intensities.
MATERIALS AND METHODS
Plant material
Eleocharis cellulosa (Cyperaceae) is a perennial grass-like sedge. It is widely distributed in the freshwater marshes of the Gulf and Atlantic coasts of the United States and Central America (Tiner, 1993
, p. 328). Its round unbranched stems, with leaves reduced to basal leaf sheaths, grow to 1 m tall. This species can tolerate high water conditions due to its rapid growth and is a dominant wet prairie species in the freshwater Everglades (Loveless, 1959
).
Seeds of E. cellulosa were collected from the oligotrophic, central area of Water Conservation Area 3A, south Florida, USA in September 2001. The seeds were germinated in unamended peat from the Florida Everglades. When the plants were about 25 cm tall, peat was carefully rinsed off the roots, and the plants were transferred to a hydroponic nursery system within an environmental growth chamber (EGC, Model M-75, Chagrin Falls, Ohio USA). The nursery unit consisted of a 10-L container with six plants. The composition of nursery solution resembled pore water in the marsh of the oligotrophic Water Conservation Area 2A (WCA-2A) (Lissner et al., 2003b
). Phosphate and ammonia solutions were added daily to these 10-L containers to compensate for nutrient uptake of the seedlings, based on the measurement of available PO43+-P and NH4+-N in the solution. The nutrient solution was renewed every 7 d. When plants were about 30 cm tall, uniform seedlings were chosen and randomly assigned to each of 36, 4-L plastic containers (experimental units).
Experimental setup
A hydroponic system was used to create a controlled redox environment (Lissner et al., 2003a
). The Eh of the hydroponic system was automatically controlled using oxidation-reduction potential (ORP) controllers, which activate and deactivate Eh control devices with high and low set points. Adjustment of the solution Eh was automatically maintained with titanium (III) citrate as a reducing agent or by bubbling compressed air as an oxidizing agent. A detailed description of the Eh controlled system can be found in Lissner et al. (2003a)
.
A randomized block design, with three phosphate levels, three Eh levels and four replicate blocks totaled 36 experimental units. The three P levels were 10, 80, and 500 µg P · L–1 (P10, P80, and P500, respectively). The three levels represent the range of P levels in surface and pore waters in WCA-2A (Koch and Reddy, 1992
). The three Eh intensities were –150, +150, and +600 mV, which are labeled by Eh–150, Eh+150, and Eh+600, respectively. The three levels represent the range of redox potential (–200 to +600 mV) at the 12.5-cm depth in soils in WCA-2A (Qualls et al., 2001
). Each experimental unit consisted of a 4-L container, containing the hydroponic nutrient solution. The plant was placed through a central hole in a lid of the container. The lid was furnished with a calomel electrode, three platinum electrodes, an inlet pipe for N2, as well as an air pump and a solenoid valve that were connected to an oxidation–reduction potential controller (for details see Lissner et al., 2003a
).
The –150 and +150 mV treatments were continuously purged with oxygen-free nitrogen gas, while the +600 mV treatment was continuously purged with compressed air. Gas flow rate was set to 35 mL · min–1 using calibrated variable-area flow meters. The +600 mV treatments were continuously aerated and thus not furnished with ORP controllers. The Eh of the +600 mV treatment was monitored every 3 d throughout the experiment with a mV meter. The ORP controllers were set at +180 (high) and +100 (low) for the +150 mv treatments, and –120 (high) and –200 (low) for the –150 mV treatments. The reducing agent, titanium citrate, was automatically added to the container via solenoid valves, when the Eh reached the high set point and stopped when Eh reached the low set point. Dead bands were set to 0 mV (Lissner et al., 2003a
, b
).
During the experiment, phosphate and ammonia solutions were added daily, based on measurements of available PO43+-P (Murphy and Riley, 1962
) and NH4+-N (LACHAT, Quickchem No. 10-107-06-3-A or B) in the nutrient tanks, to the 4-L containers to maintain a relatively stable nutrient concentration for the plants (Lissner et al., 2003b
). The pH was manually adjusted to ca. 6.5 using 1 M NaOH or 1 M HCl once or twice a day. The nutrient solution was renewed weekly. Eh of nutrient solution was adjusted to treatment level using reduced titanium citrate before renewal. Oxidized titanium citrate was added to the +150 mV and +600 mV treatment to achieve the same concentration of titanium citrate as in the –150 mV treatment. Titanium (III) citrate in the solenoid-controlled reservoir was renewed every 3 d. The experiment was carried out in an environmental growth chamber operated with a 12 : 12 h day : night photoperiod. The thermoperiod was set at a 25 : 20°C, 12 : 12 h day : night cycle.
Photosynthesis, growth, and biomass analysis
Net photosynthetic rate was determined on three young but fully developed stems with a differential carbon dioxide gas exchange system (CI-301 PS, CID, Vancouver, Washington, USA). The leaf chamber of the gas exchange system was placed at a fixed position in the environmental growth chamber using a camera tripod. To reduce variation in CO2 concentration entering the leaf chamber, air was directly drawn from the outside of the building. Air flow rate to the leaf chamber was set at 300 mL · min–1. Carbon dioxide concentration of inlet air averaged 352 ppm. Measurements were made under saturating photosynthetic photon flux density conditions with constant humidity, leaf temperature and CO2 levels (typically, 50%, 28°C, 352 ppm, respectively) and were carried out from 1200 to 1400 hours, 56 d after onset of treatments. The porosity of roots and shoots were determined with a pycnometer (Burdick, 1989
).
Shoot elongation rates (cm · d–1) were determined by measuring the changes in the length of young shoots during a 3-d period 6 weeks after the initiation of the experiment. Initial fresh mass was determined on 10 extra plants. Plants were sectioned into shoots, rhizomes and roots, and dried in a forced ventilation oven at 65°C for 72 h. Fresh weight of plants was converted to dry mass and their biomass fractions were calculated on a dry mass basis. After a growth period of 60 d, all plants were harvested. Average and maximum root length and average and maximum shoot height of each plant were measured. Plants were then rinsed in deionized water and fractionated into shoots, rhizomes, and roots. Relative growth rates (RGR, mg DW · g DW–1 · d–1) were calculated as the difference in the natural logarithm of initial and final mass divided by the experimental duration (d). The ratio between root-supported biomass (shoots and rhizomes) to root biomass (RSB/RB) was calculated. All biomass was measured and calculated on a dry mass basis.
Tissue nutrient analysis
Dead plant material was excluded from tissue samples for nutrient analyses. Nitrogen (N) concentration in shoots, rhizomes, original roots (those roots attached to plants at the beginning of the experiment) and produced roots (those roots attached to new shoots that were produced after the initiation of the experiment) were determined using a CHN analyzer (Perkin-Elmer, series II CHNS/O Elemental Analyzer 2400, Norwalk, Connecticut, USA), and phosphorus concentration was determined by inductively coupled-argon-plasma spectrometry (Thermo Jarrell Ash ICAP 61, Franklin, Maryland, USA) after digestion of 200 mg samples in concentrated HNO3 and 30% H2O2. Nutrient use efficiency (g DW · g–1 N or P) of N and P was defined as the amount of dry mass produced per gram of N or P and was calculated on a shoot basis (Chapin and Cleve, 1989
). All mass-based concentrations were converted to molar values for use in calculating molar N : P ratios on a shoot basis.
Statistical analysis
Statistical analysis was conducted with JMP software (version 5, SAS Institute, Cary, North Carolina, USA). First, all variables were analyzed by multivariate analysis of variance (MANOVA). The MANOVA test was significant for the whole model (P < 0.001). Consequently, each variable was analyzed by a 3 x 3 (redox intensity and phosphate level) factorial analysis of variance (ANOVA), replicated in 4 blocks. Data were tested for normality and homogeneity of variances to meet ANOVA assumptions and transformed if necessary. Significant differences were identified by Tukey's test, at a 0.05 probability level, unless otherwise stated.
RESULTS
Growth and photosynthesis
The effect of redox intensity on root length depended on the phosphate level (significant P x Eh interaction; Table 1). At the low P level, root length was enhanced at high Eh, while this effect was absent at low Eh (Fig. 1). Maximum root length at Eh+600 (58.4 cm) was 36–66% greater than at low and medium Eh levels (35.1 and 42.8 cm, respectively) (Fig. 1A). Average root length at Eh+600 (24.8 cm) was 48–57% greater than at the low and medium Eh level (16.8 and 15.8 cm, respectively) (Fig. 1B). At the medium and high P levels, however, no significant difference in root length was found among the three Eh levels. The treatment-level combination producing the largest maximum and average root length was P10/Eh+600 (Fig. 1).
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Phosphorus and nitrogen
Although increasing P availability and Eh significantly increased P concentration in the plant tissue, the effect of P availability was dependent on Eh (significant P x Eh interaction; Table 1). At P10, the difference in tissue P concentration was small among the three Eh intensities, while this difference among Eh intensities was significant at the higher P levels (Fig. 5). At each P level, P concentration in shoots and rhizomes did not differ significantly between Eh+150 and Eh+600. At P500, P concentration in shoots and rhizomes was significantly higher at Eh+150 and Eh+600 than at Eh–150, while P in roots at P500 was significantly higher at Eh+600 than at Eh–150 and Eh+150. Root P concentration did not differ significantly between Eh–150 and Eh+150. The treatment-level combination having the highest P content in the tissues was P500/Eh+600. Among the plant tissues, P concentration usually was the highest in shoots and rhizomes and the lowest in original roots (Fig. 5). Phosphorus use efficiency (PUE) dramatically decreased with phosphate availability, but the effect of redox potential on PUE was not significant (Table 1, Fig. 6A). Phosphorus use efficiency at P10 was 13 times that at P500 and 3 times that at P80. Phosphorus accumulation significantly increased with P availability (Table 1). Phosphorus accumulation at P500 was 2.6 times that of P80 and 12.7 times that of P10 (Fig. 6B). The effect of Eh on P accumulation was not significant (P = 0.2816).
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Environmental controls on Eleocharis cellulosa
Eleocharis cellulosa is a common species in long hydroperiod marshes of the Everglades (Stober et al., 2001
), and it usually grows in deepwater areas in the Everglades (Davis et al., 1994
). In this study, we found that Eh did not significantly influence growth variables except for root length (Table 1). Thus, contrary to our hypothesis, low Eh did not induce a major reduction in growth of E. cellulosa, cultivated in hydroponics for 2 months. Pressurized gas flow in stems of E. sphacelata increased oxygen supply to flooded roots and allows this species to grow in water depths up to 2 m (Brix et al., 1992
). Eleocharis cellulosa has the appropriate anatomy to produce such pressure gradients (Rogers, 2000
). Although we did not measure pressurized gas flow in the tested plants, the absence of significant effects of Eh on growth variables, except for root length (Table 1), indicates that convective flow of oxygen was taking place and that oxygen supply was not a limiting factor for the growth and maintenance of E. cellulose in this experiment. Therefore, E. cellulosa appears, based on these observations and our results, well adapted to deepwater or prolonged flooding. Nevertheless, low Eh, in conjunction with low P, does inhibit root extension (length), supporting the hypothesis that strongly reduced soils can inhibit root exploration for P in the unenriched, low-P Everglades.
Considerable evidence exists that phosphorus runoff from agricultural areas has been a major reason for the expansion of Typha domingensis (Personal communication) in the Everglades (Davis, 1994
; Craft et al., 1995
; Newman et al., 1996
). However, one may ask the question: do elevated phosphate concentrations affect the distribution of other Everglades species? Our results show that high phosphate levels greatly increase growth rate, biomass, and photosynthesis of E. cellulosa (Figs. 3, 4). Photosynthesis increased 3.1 times, RGR 1.6 times, shoot elongation 2.1 times, and dry mass per plant 2.2 times, when P increased from P10 to P80 or P500 (Figs. 3, 4). Busch et al. (2004)
found that the RGR of E. cellulosa increased 1.2 times when P level increased from 10 µg · L–1 to 500 µg · L–1 P level in soil rhizotrons. Typha domingensis increases in biomass and relative growth rate in response to higher P availability in the soil, while C. jamaicense and E. interstincta do not have a clear response to P availability (Newman et al., 1996
), although other studies show that C. jamaicense can respond to P enrichment (Craft and Richardson, 1997
; Miao and Sklar, 1998
; Miao, 2004
). The RGR of C. jamaicense cultivated in hydroponics for 2 months doubled and photosynthesis increased four times, when P level increased from 10 to 80 or 500 µg · L–1 (Lissner et al., 2003b
). Not only may the growth responses to P availability differ among wetland species, but the environmental conditions in which species grow may result in different responses to elevated P levels.
Although low phosphate level reduced photosynthesis, relative growth rate, and biomass, we found that low P level (10 µg P · L–1) enhanced root length of E. cellulosa. This increase in root length was greatly enhanced by Eh+600 mV (Fig. 1). These results indicate that low P level may induce root elongation of E. cellulosa, which may be an important adaptation to nutrient deficiency, and that the ability to explore low-P soil is greater in more oxidized soils with greater oxygen availability. This adaptation can help E. cellulosa obtain nutrients from deep soil in natural environments. Also, low P level (10 µg P · L–1) enhanced root porosity. This finding is supported by previous studies (Drew et al., 1989
; He et al., 1992
). In Zea mays L., phosphate-starved roots had enhanced sensitivity to ethylene and induced more aerenchyma formation. Therefore, an increase in oxygen supply caused by increased root porosity and a more aerated rooting environment can undoubtedly improve the root elongation of E. cellulosa, which is an energy-driven process, thus enabling this species to obtain phosphorus from flooded soils and ameliorate P deficiency.
Tissue P concentration for E. cellulosa increased strongly with phosphate availability and Eh of the nutrient solution (Fig. 5) as showed for C. jamaicense (Lissner et al., 2003b
). Adequate tissue P concentration for most mature crop plants is typically about 1–4 mg P · g–1 DW (Epstein, 1972
). In this study, shoot P concentrations averaged 4.8 mg · g–1 DW at P500, 1.5 mg P · g–1 DW at P80, and 0.4 mg P · g–1 DW at P10 (Fig. 5). The plants grown at P10 contained less P and had typical P deficiency symptoms such as slow growth and die-off of older leaves even in the most oxidized condition. Plants at P80 and P500 grew well and did not appear P deficient. The significant difference in net P accumulation among the three P levels (Fig. 6) strongly supports this finding. The nutrient-limitation criteria by Koerselman and Meuleman (1996)
suggest that plants with molar N : P ratios above 36 are P limited, those below 31 are N limited and those between 31 and 36 could be either N or P limited. The shoot molar N : P ratio for E. cellulosa was 101 at P10, 39 at P80, and 13 at P500 (Fig. 8). Treatment P10, therefore, was likely P limited, P500 was N limited, and P80 was either N or P limited. This finding supports the conclusion of Daoust and Childers (1999)
that the productivity and abundance of E. cellulosa in the wet prairie communities of the Everglades are regulated by P availability.
Tissue N concentration for E. cellulosa increased with phosphate availability, as showed for Cladium (Lissner et al., 2003b
), but it was not affected by Eh (Table 1, Fig. 7). Nitrogen concentration in shoots of E. cellulosa ranged from 14 to 24 mg N · g DW–1. This concentration range is higher than the N concentration (7.3 ± 0.2 mg N · g DW–1) in E. interstincta grown in soil with 50–100 µg P · L–1 and 10–1000 µg NO3-N · L–1 (calculated from Newman et al., 1996
). The non-limiting concentration for most crop plants is in the range of 15– 20 mg N · g DW–1 (Epstein, 1972
), indicating that in this study, E. cellulosa likely had a sufficient nitrogen supply. However, the increase in shoot N concentration was much smaller than the increase in shoot P in response to the elevated P treatment. At P10, shoot N concentration averaged 14.5 mg N · g–1 DW. Nitrogen luxury uptake was not observed at the low P level, although nitrogen was added in excess in comparison with P supply. Luxury uptake of nitrogen is limited when P is limiting. This finding is consistent with a previous study on three marsh species (Shaver and Melillo, 1984
).
The patterns of N and P responses of E. cellulosa to phosphate availability were similar to that of C. jamaicense, but the effects of redox potential on tissue N and P of E. cellulosa were very different from Cladium (Lissner et al., 2003b
). For Cladium, the uptake and N and P use efficiencies were governed by both P availability and redox intensity. In contrast, for E. cellulosa, tissue P concentration was affected by P availability and redox intensity, while N uptake and use efficiency were governed only by P level (Fig. 6).
The growth of E. cellulosa was not significantly affected by redox intensity, which is quite different from C. jamaicense. Low redox intensity significantly reduced C. jamaicense root growth and root biomass (Lissner et al., 2003b
). The photosynthetic rate, leaf elongation, and relative growth rate of C. jamaicense were generally lower at Eh–150 than at Eh+150 or Eh+600 (Lissner et al., 2003b
). Cladium jamaicense biomass was the lowest at an Eh of –200 mV and the highest at an Eh of +250 mV in an experimental range of –200 to +500 mV (Kludze and DeLaune 1996
; Pezeshki et al., 1996
). Because this species has maximum growth at +250 mV, C. jamaicense appears better adapted to moderately reducing conditions than to fully oxidized conditions (Kludze and DeLaune, 1996
). In this study, the growth and biomass of E. cellulosa was not significantly affected by a low Eh (–150 mV), except for root length. In a recent study, shoot height of E. cellulosa grown with 54 cm of soil-flooding, which resulted in a low redox potential, was significantly higher than that of plants in 5 cm soil flooding, which resulted in relatively higher redox potential, although shoot biomass between them did not significantly differ during an experimental period of 80 wk (Edwards et al., 2003
). Busch et al. (2004)
reported that flooding with 45 cm of water significantly increased the biomass and relative growth rate of E. cellulosa, compared to a drained control. It appears that E. cellulosa is well adapted to redox intensities between –150 and +600 mV and to relatively high water levels that can create low redox potentials.
The difference between the growth and nutrient responses of E. cellulosa and C. jamaicense to redox intensity is interesting. Eleocharis cellulosa mainly occurs in wet prairie communities in open water areas (Vaithiyanathan and Richardson, 1999
) and is less frequent in C. jamaicense communities (Jordan et al., 1997
). The sites where E. cellulosa is present have an inundation frequency of 53–96% and a water depth of 14– 62 cm (David, 1996
). Eleocharis cellulosa was the only species positively associated with water depth among eight species in Shark slough marshes (Busch et al., 1998
). These results are supported by a recent study in which flooding resulted in large increases in relative growth rate, canopy height, and aboveground and belowground biomass of E. cellulosa (Busch et al., 2004
). In contrast, high redox intensity (low Eh) significantly decreased the relative growth rate, leaf elongation, biomass, and photosynthesis of Cladium (Pezeshki et al., 1996
; Lissner et al., 2003b
). Also, the cover and density of C. jamaicense was negatively associated with water depth in Shark Slough marshes (Busch et al., 1998
). These differences in the growth response of the two species are likely due to differences in the ability to transport oxygen to their root systems. Eleocharis cellulosa has a very high root porosity (a measure of air space in roots) of about 50% (in this study; Busch et al., 2004
), which is much higher than that of C. jamaicense at 10% (Chabbi et al., 2000
). Also, Eleocharis cellulosa, as is true for other species of Eleocharis, likely has a convective flow of O2, while C. jamaicense does not (Sorrell et al., 2002
).
Implications for species success in the Everglades
How can our results help explain the observation that wet prairie communities, dominated by E. cellulosa, have been replaced by C. jamaicense in certain regions (Davis et al., 1994
)? A proposed hypothetical model (Fig. 9) provides further insight. Our research and others cited herein suggest that P availability and hydrologic regime (duration and depth of inundation) drive changes in vegetative communities of the Everglades. The natural habitat of E. cellulosa and C. jamaicense is oligotrophic freshwater marshes. Eleocharis cellulosa commonly occupies extensively flooded and deepwater areas, while C. jamaicense usually occurs at sites covered with relatively shallow surface water (Loveless, 1959
). It is generally accepted that the relative dominance of Cladium and Eleocharis under ambient P conditions is dependent on the hydrologic regime. Cladium dominates over Eleocharis in short-hydroperiod areas. Phosphorus enrichment promotes the growth of both Eleocharis and Cladium (Figs. 3, 4). However, the relative success of these two species cannot be evaluated without considering T. domingensis that has dramatically expanded in the Everglades in recent years (Davis, 1994
). Typha domingensis is able to dominate Eleocharis and Cladium under P-enriched and flooded conditions (Newman et al., 1996
). Cladium and Typha occur in mixtures under short-hydroperiod and P-enriched conditions, but eventually Typha will replace Cladium and create a monospecific pure stand (Fig. 9).
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) or low redox potential (in this study). In contrast, C. jamaicense would perform better in shallow water and moderate Eh conditions (Jordan et al., 1997
; Lissner et al., 2003b
) and would likely be more competitive under shortened hydroperiod conditions. The conversion of wet prairie/ slough to sawgrass habitat may have resulted from the many hydrological alterations caused by drainage canal construction and water management practices (Davis et al., 1994
; Ogden, 2003
). Field observations also demonstrate the hydrological effects on vegetation change in Shark River Slough (Kolipinski and Higer, 1969
; Davis et al., 1994
; Olmsted and Armentano, 1997
). In northern Shark River Slough, wet prairie species have been replaced by sawgrass since 1940, and this vegetation change paralleled hydroperiod reduction (Kolipinski and Higer, 1969
). Therefore, the restoration of the natural hydrology is necessary to maintain wet prairie/slough communities in the Everglades.
FOOTNOTES
1 The authors thank the South Florida Water Management District for funding the study. We also thank Qinxian Lin, Matt Slocum, Lee Stanton, Pamela Weisenhorn, and Joshua Roberts for assistance during harvest, and Sue Newman, Fred Sklar, and Carl Fitz for their comments on the manuscript. 
5 Author for correspondence (e-mail: imendel{at}lsu.edu
), phone: 1-225-578-6425, fax: 1-225-578-6423
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