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Ecology |
2Department of Plant Ecology, University of Aarhus, Nordlandsvej 68, DK-8240 Risskov, Denmark; 3Wetland Biogeochemistry Institute, Louisiana State University, South Stadium Road, Baton Rouge, Louisiana 70803 USA; 4U.S. Geological Survey, National Wetlands Research Center, 700 Cajundome Boulevard, Lafayette, Louisiana 70506 USA; 5South Florida Water Management District, P.O. Box 24680, 3301 Gun Club Road, West Palm Beach, Florida 33406 USA
Received for publication July 30, 2002. Accepted for publication November 21, 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSLITERATURE CITED |
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Key Words: Cladium jamaicense • Cyperaceae • Everglades • micronutrients • nutrient acquisition • nutrient allocation • nutrient use efficiency • photosynthesis • sawgrass • Typha domingensis
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSLITERATURE CITED |
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; Light and Dineen, 1994
; McIvor et al., 1994
; Newman et al., 1998
; Miao and DeBusk, 1999
).
Much of WCA-2 is characterized by peat soils with varying marl content overlying a limestone plateau. The peat is rich in calcium carbonate, and the soils thus possess a high capacity for P precipitation (Koch and Reddy, 1992
; Richardson and Vaithiyanathan, 1995
). Indeed, undisturbed WCA-2 soils are extremely low in dissolved reactive phosphate (2–14 µg P/L), and P has been demonstrated to be the limiting plant nutrient (Davis, 1991
; Urban et al., 1993
; Richardson et al., 1999
). A number of field and laboratory studies suggest that T. domingensis is competitively superior to C. jamaicense when the nutrient supply increases (Steward and Ornes, 1975b
; Davis, 1991
, 1994
; Newman et al., 1996
; Craft and Richardson, 1997
; Miao and Sklar, 1998
; Lorenzen et al., 2001
). Relative to T. domingensis, C. jamaicense has less plasticity in growth rate to increased nutrient inputs, has a low demand for nutrients, depends less on a high uptake affinity in an infertile environment, and has a high retention capacity for acquired resources (Newman et al., 1996
; Richardson et al., 1997a
).
Soil Eh (redox potential) of –100 to –200 mV is common in the Everglades, and resistance to oxygen deficit may be an important factor regulating the distribution of C. jamaicense (Kludze and DeLaune, 1996
). Soil Eh is governed by hydrology, which in the Everglades system has been dramatically altered during the last century (Walters, 1992
; Fennema et al., 1994
; Light and Dineen, 1994
). Construction of drainage canals and diking has fragmented remnant Everglades wetland into four major hydrological units (Davis and Ogden, 1994
), and human regulation of the hydroperiod has disrupted the natural, erratic frequency and intensity of flooding and drought (Loveless, 1959
; Steward and Ornes, 1975b
; Richardson et al., 1997b
; Newman et al., 1998
). The periodic flooding of the Everglades dictates that plants must be adapted to these conditions. Pressurized bulk flow, a means of internal underground aeration in some plants, was undetectable in C. jamaicense (Sorrell et al., 2000
), suggesting that this species relies on diffusional processes to supply belowground organs with oxygen. Cladium responds to prolonged waterlogging by forming coarser primary roots with fewer or no laterals (Conway, 1936
) probably in an effort to increase downward diffusion of oxygen as well as to reduce its consumption. The production of coarse roots in response to oxygen deficiency increases cross-sectional air spaces, which in turn increase flooding tolerance (Naidoo and Naidoo, 1992
; Marschner, 1995a
). This morphological adaptation indicates that a stress avoidance mechanism operates in C. jamaicense, compensating for the lack of pressurized bulk flow. However, an overall low capacity of C. jamaicense to aerate roots and rhizosphere in flooded soils is indicated by a shallow rooting depth, high alcohol dehydrogenase activity, and high alcohol diffusion to the root medium, and points to a relatively low flood tolerance for C. jamaicense (Chabbi et al., 2000
).
This study was conducted to quantify the interactive effects of P availability and redox intensity on growth, nutrient relations, and biomass allocation of C. jamaicense. We hypothesized that low Eh, imitating permanently flooding conditions, reduces growth of C. jamaicense across a broad range of P availabilities. We present results quantifying the growth response of C. jamaicense at Eh levels ranging from –150 to +600 mV and phosphate levels ranging from 10 to 500 µg P/L during a 2-mo experimental period.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSLITERATURE CITED |
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). The peat was carefully rinsed off the roots when the plants were 15–20 cm tall (12 wk old), and the plants were transferred to a hydroponic nursery system within the experimental growth chamber (Environmental Growth Chambers, Model M-75 [=uipped with Sunbrella fixtures], Chagrin Falls, Ohio, USA). Each growth unit of the nursery consisted of a 10-L container with eight plants. The chamber was operated with a 12 : 12 h day : night photoperiod with 10 h of maximum light and 1 h transition periods of reduced light. Because of the proximity of the plants to the lamps, there was a gradient in light intensity from 2000 µmol · m–2 · s–1 PAR at 1 m above shoot base level to 1200 µmol · m–2 · s–1 PAR at shoot base level, the range 50% lower during transition periods. The thermoperiod was set at 27° : 20°C 10 : 14 h day : night cycles.
Nutrient solutions
The composition of the basic nursery solution (Table 1) was designed to resemble pore water concentrations in the Cladium marshes of the oligotrophic Water Conservation Area 2A (B. Lorenzen, University of Aarhus, Denmark, unpublished data). The P-addition solution containing P (as orthophosphate), K, Ca, SO4, and micronutrients was added daily in 40 µg PO4-P/L increments during the establishment phase. The nitrogen-addition solution containing NH4+-N, Fe, and SO4 was prepared daily and added relative to plant uptake. Both addition solutions were designed to compensate for nutrient uptake of C. jamaicense, thus restoring daily the ionic composition of the nutrient solution. PO4-P and NH4+-N were analyzed colorimetrically using the ammonium molybdate method (Murphy and Riley, 1962
) and the automated phenolate method (Method 350.1, EPA-600 4-79-020, U.S. Environmental Protection Agency, 1979), respectively. Transpired water was replenished daily with deionized water, then pH was adjusted to 6.5. The solution was completely renewed every week. Five days prior to plant transfer to the experimental containers (plant height ca. 45 cm) phosphate addition was reduced to 10 µg P · L–1 · d–1, to deplete any pool of excess P in the plants.
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), while compressed air was used as an oxidizing agent. Titanium citrate was prepared under an N2 atmosphere according to the method of Zehnder and Wuhrmann (1976)
. Each experimental unit consisted of a 4-L bottle serving as a tank for the nutrient solution. The lid was furnished with a central hole through which a C. jamaicense plant was placed. The lid was also mounted with (1) a calomel electrode, (2) three replicate platinum electrodes of the welded type (Patrick et al., 1996
), (3) an inlet pipe terminating in a bubble stone carrying air or nitrogen gas for mixing and purging, and (4) an inlet pipe from an air pump connected to the ORP controller. A solenoid valve connected to the ORP controller was used to control the addition of titanium citrate using a 15-cm piece of 0.03-cm internal diameter PTFE tubing terminating in the nutrient solution. Flow was generated by gravity using a 125-mL plastic bottle as a titanium citrate reservoir. A full description of the system, as well as an evaluation of its performance, is given in Lissner et al. (2003)
.
Experimental setup
The experimental design was a randomized block with three phosphate levels (10, 80, and 500 µg P/L, designated P10, P80, and P500, respectively), three Eh levels (–150, +150, and +600 mV), and four replicates per treatment. The nutrient solution for 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. Nitrogen- and airflow rates were set to 35 mL/min using calibrated variable-area flow meters. Because the experimental units in the fully oxidized, +600 mV treatment were continuously aerated they were not furnished with ORP controllers. The Eh levels of the +600 mV treatment were monitored every 3 d throughout the experimental period using a portable voltmeter (Digi-Sense, Cole-Parmer, Vernon Hills, Illinois, USA) and averaged +601 mV (SD = 41 mV; n = 228). The Eh of the nutrient solution was found to decrease 50 mV per pH unit (Lissner et al., 2002
). Since Eh of the +600 mV treatment was not controlled, changes in pH from plant NH4+ uptake caused Eh to increase between the daily pH adjustments. The diurnal fluctuations in Eh were greater towards the end of the experiment when plants had developed more root biomass but never exceeded 100 mV for large plants. The Eh was gradually lowered for the medium and low redox treatments during a 3-d acclimation period preceding the onset of the experiment. The final experimental set point settings for the ORP controller-relays were +180 (high) and +100 (low) for the +150 mV treatments and –120 (high) and –200 (low) for the –150 mV treatments. Dead bands (hysteresis bands) were set to 0 mV. The +150 and –150 mV treatments also fluctuated ca. 100 mV between control events because of the 80 mV windows between set points and lag time effects. Thus, for the +600 mV, +150 mV, and –150 mV treatment levels, the Eh ranged from +550 to +650 mV, +200 to +100 mV, and –100 to –200 mV, respectively.
When the Eh reading rose above the high set point, the solenoid valve was activated and titanium citrate was added to the solution (ca. 0.05 mL/min) causing Eh to decrease. Whenever Eh readings fell below the low set point, an air pump was activated causing Eh to rise. Phosphate taken up by the plants was replenished every 12 h using a deoxygenated P-addition solution (Table 1). Addition volumes were calculated every 2–4 d and were based on depletion rates determined from phosphate measurements using the ammonium molybdate method. Ammonium and FeSO4 were added daily based on NH4+ uptake using the nitrogen-addition solution (Table 1). The pH was adjusted manually once or twice daily to ca. 6.25 by adding 1 mol/L NaOH or HCl. The nutrient solutions were renewed weekly using deoxygenated solutions for the medium and low Eh treatments. Reduced titanium citrate was used to adjust Eh level of nutrient solution to treatment level before renewal. Oxidized titanium citrate was added to the +150 mV and +600 mV treatments to achieve the same total concentration of titanium citrate across treatments. Titanium citrate in the reservoirs was renewed twice weekly.
Growth and biomass analysis
Initial fresh masses of 36 randomly selected plants from the nursery stock were determined using a standardized weighing procedure, and the plants were randomly assigned to experimental units. To estimate the initial dry mass of each experimental plant and their biomass fractions, the initial fresh mass was determined for another 10 randomly selected plants separated into leaves, shoot bases, rhizomes, and roots. Shoot bases comprised the disk-shaped stem and the slightly swollen basal parts of the leaves and was delineated from the leaves at the narrowest point where the color changed from reddish-purple to green. The average fresh-to-dry-mass ratio of the biomass fractions was calculated after drying to a constant mass in a forced ventilation oven at 65°C.
Each replicate was harvested blockwise in random order after growing 9 wk. Shoot lengths of each plant were measured. The maximum root length and the maximum lengths of lateral roots for four primary roots of each plant were recorded. Plants were then rinsed in deionized water and divided into leaves, shoot bases, rhizomes, coarse, and fine roots and dried for dry mass determination. Coarse roots were not present at the experimental start and differed from fine roots by having few or no laterals (Conway, 1936
) and by being thicker in diameter (1.5–4 mm as opposed to <1.5 mm for fine roots). A third root type, cluster roots, was only observed for P10 plants and was grouped together with fine roots during sorting. Average relative growth rates [RGR, measured in milligrams of dry mass per gram of dry mass per day] were calculated as the difference in the natural logarithm of initial and final dry masses divided by days. Based on the biomass fractions, the ratio between root-supported biomass (leaves, shoot bases, rhizomes) to the root biomass (RSB/RB) was calculated.
Leaf elongation rates (in centimeters per day) were determined 6 wk after onset of treatments by measuring changes in the length of two consecutive young leaves per replica during a 3-d period. Rates of net photosynthesis were determined with a differential carbon dioxide gas exchange system (model CI-301 PS, CID, Vancouver, Washington, USA) using a leaf chamber (model CI-301LC-2 Open System Chamber, CID) with an exposed area of 6.5 cm2. This chamber was placed in the growth chamber in a fixed position at mid-canopy (1300 µmol · m–2 · s–1 PAR) using a camera tripod. To limit variation in CO2 concentration entering the chamber, air was drawn from outside the building. A 20-L buffer container in the inlet system provided further limits to CO2 variability and also acted as a humidifier. Humidity of air entering the chamber was maintained at 60–65% relative humidity by adding variable amounts of wet paper towels to the buffer container. Flow rate to the leaf chamber was set at 300 mL air/min. Leaf temperatures were maintained at ambient growth chamber temperature (27 ± 1°C). Carbon dioxide concentration of inlet air averaged 352 ppm. Measurements were started 2 h after the onset of the photoperiod ca. 60 d after onset of treatments and lasted for 4 d, with one block measured per day. Net CO2 assimilation rates were measured on the first, second, and third youngest emerged leaf. Intact, single leaves were clamped at midleaf position and three sets of photosynthetic rates were measured by integrating over 1-min periods. Thus, nine measurements were recorded and averaged for each replicate before statistical analysis.
Tissue nutrients
Dried plant tissue was ground, and the nitrogen content of leaves, shoot bases, rhizomes, coarse roots, and fine roots was determined using a CN analyzer (Perkin-Elmer, Series II CHNS/O Analyzer 2400, Norwalk, Connecticut, USA). Nitrogen uptake (in milligrams per plant) and the proportion of total plant N in shoot bases (in percentages) were calculated as well as the inverse nitrogen concentration (nitrogen use efficiency [NUE]). The concentrations of P, K, Ca, Mg, Mn, Mo, Cu, Zn, and Fe for the various plant parts were determined by inductively coupled argon-plasma spectrometry (Thermo Jarrell Ash ICAP 61, Franklin, Maryland, USA) after digestion of 200 mg samples in HNO3 and H2SO4. Dead plant material and submerged ramets were excluded in the analysis. Initial concentrations of elements in the plant parts were estimated using values averaged from the 10 randomly selected plants from the nursery stock. Phosphorus uptake (in milligrams per plant), the proportion of total plant P in shoot bases (in percentages), and the inverse P concentration (phosphorus use efficiency [PUE]) were calculated.
Statistical analyses
All variables were analyzed using multivariate analysis of variance (MANOVA; JMP v. 3.1, SAS, 1995). The multivariate model applied to the factorial randomized block design was Y = f(block, redox intensity, phosphate level). Most variables were logarithmically transformed to ensure normality of error terms prior to testing. The MANOVA test was significant (P < 0.001) for the interaction. Two-way ANOVAs were subsequently carried out for each independent variable to identify significant treatment effects. No adjustments of 
were undertaken. Fisher's least-square-difference procedure was used to separate means at the = 5% level.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSLITERATURE CITED |
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Table 4 also shows total P accumulation (in milligrams of P per plant) based on initial and final dry mass and P concentrations. Phosphorus accumulation was reduced by low redox potential, but increased with phosphate availability (Table 3). Values ranged from –0.41 mg P/plant representing a net loss of P during the experimental period to a net accumulation of 144 mg P/plant.
Treatment effects on tissue nitrogen content and NUE were less dramatic than for tissue phosphorus and PUE (compare Tables 4, 5). In general, tissue nitrogen concentrations increased twofold across the range of phosphate treatments (Table 5). Except for coarse roots, lowest tissue nitrogen within each phosphate level was generally associated with low Eh of the nutrient solution. As was the case with P, percentages of total plant nitrogen in shoot bases did not relate to P availability or Eh (Tables 3, 5). Total nitrogen accumulation (in milligrams of N per plant) was 15-fold greater at P500 than at P10 and was ca. twofold greater at +600 mV than at –150 mV within each phosphate level (Table 5).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSLITERATURE CITED |
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) and is consistent with findings of other C. jamaicense studies (Newman et al., 1998
; Lorenzen et al., 2001
).
Relative growth rate at P10 was higher than expected from photosynthetic and leaf elongation rates. This discrepancy may be caused by an initially high P content in the plants, which was higher (averaged 2.3 mg P/g dry mass [DM]) than the critical level for C. jamaicense (0.7 mg P/g DM [Steward and Ornes, 1983
]). Utilization of reserve P at the P10 treatments may therefore have accelerated initial growth rates until internal P pools were depleted when the reported values of leaf elongation and photosynthesis were measured at 6 and 9 wk, respectively, after onset of treatments. Although this initially high P content in the P10 plants may have elevated the RGR in this treatment, the RGR was still significantly lower than for the P80 and P500 treatments.
Kludze and DeLaune (1996)
reported maximum growth for C. jamaicense at an intermediate Eh level (+250 mV) suggesting that C. jamaicense is better adapted to moderately reducing conditions than to fully oxidized conditions. In the present study, this situation was seen only for C. jamaicense grown at high P availability (P500), as RGR, leaf elongation rates, and photosynthesis were similar at +150 and +600 mV. In contrast, C. jamaicense plants grown at intermediate (P80) and low P availability (P10) generally had lower growth at +150 mV than at +600 mV. The growth responses obtained in this study thus indicate that P limitation shifts the optimum Eh level to higher values, suggesting that the Eh and nutrient optima are not independent.
The growth data presented in Fig. 1 also shows that the decreased growth rate in strongly reduced conditions can be compensated for by elevating the phosphate availability when P is limiting growth. The higher phosphate levels are needed to balance a reduced P uptake and/or a reduced capacity to conserve P when Eh decreases. Growth in reduced soils, a common result of prolonged flooding, may thus reduce the competitive ability of C. jamaicense in nutrient-poor habitats and favor other wetland plant species in which growth is relatively less reduced at low redox potentials. Since C. jamaicense has a low inherent growth capacity, it may be out-competed in nutrient-enriched environments as well by species exhibiting higher growth capacity. Increased hydroperiod and nutrient enrichment may thus independently exclude C. jamaicense from growth sites. It should be noted that nutrient enrichment is likely to result in a greater degree of soil reduction because of the direct effect of nutrient enrichment on nutrient-limited microbial metabolism and the greater production of organic material serving as substrate for bacterial breakdown. The relative importance of the opposing effects of decreased Eh and increased nutrient availability on the growth of C. jamaicense in Everglades soils will depend on the changes in absolute values for both parameters.
Biomass allocation
Biomass partitioning can be considered a growth optimization process by which a balanced growth of both roots and shoots leads to an optimal allocation strategy with respect to the external environment (Mooney and Winner, 1991
). This study demonstrated an approximate 2.5-fold increase in the ratio between root-supported tissue and root biomass (RSB/RB) for C. jamaicense in response to P availability. This relatively small increase in RSB/RB is characteristic of slow-growing plant species, which typically exhibit less than a threefold variation in root-to-shoot ratio over a nutrient gradient (Nassery, 1970
; Christie and Moorby, 1975
). However, RSB/RB ratios in another hydroponic study involving C. jamaicense (Lorenzen et al., 2001
) were much higher than in the present study (RSB/RB ranged from 5.6 to 8) and did not relate to P availability, in contrast to the present study. Also, Miao and Sklar (1998)
found no relation between biomass allocation and nutrient availability. The authors presented biomass data for three stands of C. jamaicense along a nutrient gradient in the Everglades for which similar biomass allocation ratios (RSB/RB) of ca. 4 can be calculated. Thus, both the absolute values of RSB/RB and the modification of RSB/RB by C. jamaicense in response to P availability are debatable. Therefore, RSB/RB ratios of C. jamaicense may be influenced by factors other than P availability, making comparisons of RSB/RB ratios of different studies difficult.
The effects of Eh on RSB/RB biomass ratios were less pronounced than that of P availability. Low Eh resulted in increased RSB/RB indicating that a reduction in root biomass was accompanied by a relatively smaller reduction in shoot biomass. The impact of biomass ratios on nutrient acquisition is difficult to evaluate as both nutrient availability and Eh modify root morphology. The relatively smaller root biomass at low redox and the change in root morphology towards coarser roots point to much lower root surface area for a given plant biomass at low Eh. It is possible that this lower root surface area may be the main factor behind the observed negative effect of low redox on growth. A different response, however, was found for C. jamaicense grown at Eh levels ranging from –200 to +500 mV (Kludze and DeLaune, 1996
). At –200 mV, both root and shoot growth was nearly halved when compared to the optimum Eh level, resulting in a relatively narrow range in root to shoot ratios (3.0–3.7) across Eh levels.
Chronic P stress has been found to increase root length and root dry mass and to shift root morphology towards finer roots (Marschner, 1995b
). Combined, these responses can be considered a strategy to enhance P acquisition (Chapin, 1991
). In accordance, C. jamaicense responded to low P availability by producing longer primary roots, a result in agreement with findings of Lorenzen et al. (2001)
. These authors also found that low P stimulated allocation of biomass into C. jamaicense laterals and increased the proportion of finer roots, resulting in a larger nutrient-absorbing root surface area. The present study indicated that these responses were counteracted by low Eh, causing allocation of biomass into shorter, coarser primary roots with fewer and shorter laterals. Rooting density is likely to be reduced for C. jamaicense when subjected to prolonged flooding as a consequence of the development of coarser roots (Chabbi et al., 2000
) and decreased root biomass. While the diffusion rate of oxygen to the roots may increase by the change in root morphology, the potential to absorb P is likely reduced as a result of the reduced rooting density. Phosphate is considered poorly mobile in soils, and transfer to the root is likely to limit uptake rather than absorbing capacity so that uptake is governed largely by rooting density (Bowen, 1982
). Mathematical models have indicated that biomass investment in coarse roots is inefficient for nutrient uptake (Boot, 1990
). Uptake of poorly mobile or immobile nutrients therefore is probably reduced in soils when Eh is low. Low Eh may therefore have more adverse effects on the vigor of C. jamaicense in natural, nutrient-poor soils than indicated by hydroponic experiments.
Elemental concentrations of plant tissue
Critical P levels in mature leaf tissue of crop plants typically range from 2 to 4 mg P/g DM (Jones, 1998
). In this experiment, only plants grown at P500 contained P concentrations in leaves comparable to this range (2.2–3.3 mg P/g DM). Plants grown at P80 contained much less leaf P (0.64 mg P/g DM at +600 mV) but did not exhibit typical P deficiency symptoms, such as slow growth and die-off of older leaves (Jones, 1997
). In fact, at +600 mV, RGR, photosynthesis, and leaf elongation rates did not differ between P80 and P500 plants, indicating that growth of C. jamaicense reached a maximum at phosphate concentrations of ca. 80 µg P/L and that higher external phosphate levels cannot be exploited relative to increased growth. Critical values for plant P in leaf tissue of C. jamaicense have previously been estimated at 0.7 mg P/g DM (Steward and Ornes, 1983
), a concentration close to the 0.64 mg P/g DM measured for P80/+600 mV plants of this study. These findings suggests that the range for P sufficiency is much lower for C. jamaicense than for crop plants, underlining that C. jamaicense is well adapted to a low-P environment. Concentrations of tissue P were lower for both P80 and P500 plants at –150 and +150 mV than at +600 mV, and growth was reduced as well. Thus, P uptake appears to be impeded by low redox intensity, probably because of changes in root morphology and P metabolism.
Phosphorus content of mature leaves of P10 plants were much lower than the estimated critical value of 0.7 mg P/g DM, and consequently growth was slow. Because P is fairly mobile in the plant (Jones, 1998
), deficiency symptoms initially occur in older leaves because P is translocated to growing leaves. At the onset of the experiment, some growth at this P level probably relied on initially high plant P content after which the plants had to balance their biomass to the low supply rate. The negative net P uptake for plants grown at P10/–150 mV and P10/+150 mV indicate that C. jamaicense was unable to maintain tissue P homeostasis at these treatment combinations. This negative net P uptake would probably have been less dramatic if the plants were acclimated to a low rate of P supply at the onset of the experiment.
Leaf tissue concentration of plants grown at P10 (0.21–0.23 mg P/g DM) are comparable to values measured for C. jamaicense at unenriched sites of the Everglades (Steward and Ornes, 1975b
; Koch and Reddy, 1992
; Craft et al., 1995
; Richardson et al., 1999
). These values are well below the critical level of 0.6–0.7 mg P/g DM, supporting the contention that the Everglades system is P deficient relative to C. jamaicense requirement. However, this species may still be the best competitor among the other plant species when phosphate is scarce. Cladium jamaicense may also rely on pulsed additions of P and a subsequent high retention capacity for long-term persistence in the Everglades (Steward and Ornes, 1975b
).
While low Eh in the P10 treatments did not affect the P concentrations of rhizomes, shoot bases, and leaves, the P content of coarse roots and fine roots was two- and sixfold lower for the –150 mV and +150 mV treatments, respectively, in comparison to the +600 mV treatment. This lower P was probably partly related to some root tissue being dead or dying and to P being translocated to living tissue or lost to the nutrient solution.
The P80/+600 mV treatment combination may represent the most ideal combination of phosphate availability relative to other nutrients and redox intensity. Plants in this treatment exhibited high growth rates and had the highest uptake (by percentage) of added P and N. It is interesting to note that these apparently optimum conditions for C. jamaicense, at least with respect to phosphate availability, are similar to those of the nutrient-enriched areas in the Everglades, where this species is being replaced by T. domingensis. Thus, some factor, probably competition from other plant species, appears to confine C. jamaicense to sites of suboptimal P availability.
The shoot bases of C. jamaicense may serve as a nutrient storage organ (Miao and Sklar, 1998
), but the percentage of total plant nutrients (P and N) in the shoot bases was low (6–9% at P500) and did not differ between treatments. Rather P and N increased in all tissue fractions with increased nutrient availability, indicating that P and N are stored in all organs. This study therefore does not support that shoot bases of C. jamaicense serve as nutrient storage organs in the vegetative growth phase. The high general nutrient concentrations in shoot bases may reflect that this is a site rich in meristematic tissue with a high metabolic activity and nutrient demand.
Slow-growing, low nutrient status species generally have higher PUE than faster-growing species (Bowen, 1982
; Davis, 1991
). A high PUE and nutrient-absorbing modifications such as cluster roots are essential in coping with low nutrients (Neumann et al., 1999
). In accordance, we found that maximum growth rates of C. jamaicense were associated with PUE values as high as 1000 g DM/g P. Both P stress and redox intensity were found to increase PUE. The maximum PUE value sustaining growth of C. jamaicense is probably close to 2300 g DM/g P (P10/+600 mV); plants grown at lower redox at this P level lost P during the experimental period and may not have survived for extended periods.
The nitrogen concentration of leaf tissues in this study ranged from 10 to 20 mg/g DM. These values are somewhat higher than N concentrations measured in leaves of C. jamaicense in the Everglades, which average 6 mg/g DM (Steward and Ornes, 1975a
, b
). The sufficiency range for plants is in the range of 20–50 mg N/g leaf DM (Marschner, 1995c
), indicating that C. jamaicense has a lower nitrogen requirement than most plants because this study demonstrated high RGR for plants averaging 16 mg N/g leaf DM.
The uptake of N and P were not independent despite that nitrogen was added in excess to P across the range of phosphate concentrations offered to the plants. However, nitrogen concentrations in leaf tissues were much less sensitive (twofold) to the treatments than P (50-fold). Shaver and Melillo (1984)
noted for three species of marsh graminoids that luxury uptake of nitrogen is limited when P is limiting and that the N/P ratio was correlated with the N/P supply ratio. The decrease in N content with decreasing phosphate availability does not therefore reflect lower N availability at low P availability, which otherwise would have confounded treatment effects.
The significant interaction for all plant parts indicated that the effects of redox intensity on nitrogen content was small or absent at P80 and P500. At P10, nitrogen content was reduced about 20–50% at –150 mV compared to +600 mV. The highest reduction was measured for root tissues and may represent an overestimation because a fraction of the root tissues may have consisted of dead biomass with reduced N content. Redox potential appears therefore to have little effect on nitrogen uptake for C. jamaicense when nitrogen is added in excess of P.
In this study, leaf K, Mg, and Ca was well within the sufficiency range (Jones, 1998
) indicating that no deficiency of these ions affected growth. Low Eh about halved the Ca and Mg content of the leaves and may reflect that the number of uptake sites is likely to be fewer at low Eh because fine roots to a large extent are replaced by coarse roots with fewer laterals.
Iron is subject to changes in oxidation state as a function of redox conditions. In this experiment, iron was added as Fe2+, which is relatively stable below ca. +150 mV at pH = 6 (Kemp, 1989
). However, oxygen loss from the roots mediated a change in oxidation state of iron, a process that is known to cause precipitation of oxidized Fe compounds (iron plaque) on root surfaces (Mendelssohn and Postek, 1982
; Taylor et al., 1984
). The formation of iron plaque was most pronounced for the +150 mV treatments followed by the –150 mV and +600 mV treatments (Table 6), suggesting that Fe2+ may have been oxidized in the water column in the +600 mV treatments. Despite that some iron was oxygenated and considering that Fe2+ generally is taken up preferentially to Fe3+ (Marschner, 1995d
), the concentration of iron in leaves was similar across treatments and higher than the sufficiency range (50–75 µg Fe/g DM) as listed for plant leaves in Jones (1998)
. Although the metabolically active fraction of iron in the roots remains unknown, the relatively high and uniform iron concentration of leaves suggests that the roots and remaining plant parts were not iron deficient. Thus, neither Eh or P availability affected leaf Fe in C. jamaicense.
Like iron, manganese is a metal that changes in oxidation state as a consequence of the redox conditions of the rooting medium (Gambrell, 2001
). Manganese (Mn2+) is readily oxidized to Mn3+ and Mn4+ at Eh above 350–450 mV (Marschner, 1995a
). Plants take up Mn in the Mn2+ ionic form, but judging by the fairly high Mn contents at +600 mV, no significant oxidation of Mn2+ took place in the aerated treatments. The low Mn content in leaves at –150 mV is likely to be explained by precipitation of MnCO3 (rhodocrosite), which is expected to form as the system becomes reduced (Schwab, 1981 in St-Cyr and Crowder, 1990
). Formation of MnCO3 at –150 mV may thus have reduced the plant-available Mn significantly. However, the low levels of leaf Mn did not impair growth because only the P10 plants had low photosynthetic rates at –150 mV.
In the present study, leaf concentrations of Cu (1.9–7.4 µg/g DM) and Zn (62–154 µg/g DM) were much higher than measured for C. jamaicense leaves in the Everglades (Cu, 0.07–1.03 µg/g DM; Zn, 3.9–9.3 µg/g DM) (Vaithiyanathan and Richardson, 1997
). The relatively high leaf concentration of both nutrients indicate that no Cu and Zn deficiencies were present in this study even though uptake of both elements was reduced by ca. 50% at low Eh. Copper and Mo were found in up to 10 and 30 times higher concentrations, respectively, in the roots than in the leaves, supporting the general finding in the literature that Cu and Mo have low mobilities in plants (Jones, 1998
). The concentrations of Mo in the leaves of C. jamaicense were also well within or above the critical deficiency range (Marschner, 1995d
). Possible factors responsible for the lower Mo content of leaf and root tissues at the low redox treatments compared to the medium and high redox treatments may include changes in root morphology induced by low redox, resulting in fewer sites for active uptake or reduced metabolically controlled uptake. Molybdenum may also become less available because of reduction of the molybdate oxyanion, Mo+VIO42– to Mo+III(OH)3.
The contents of some micronutrients (Mn, Zn, Mo, Fe) were relatively low at P80/+150 mV in comparison to other treatment combinations and may have been diluted from rapid growth. These nutrients were provided relative to P uptake, which at the P80/+150 mV treatment was taken up most efficiently among the treatments.
The low requirement for Mn, Cu, and Zn as well as P and N, as discussed earlier, indicates that Cladium jamaicense is a low nutrient status species. The concentrations of N, K, Ca, Mg, Mn, Zn, Mo, and Cu were lower for plants grown at –150 mV than for plants grown at +600 mV. Nevertheless, leaf concentrations of all measured nutrients (except P) were within or above the general sufficiency ranges reported for plants.
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6 Author for reprint requests (imendel{at}lsu.edu
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