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2 Lehstuhl für Bodenschutz und Rekultivierung, Brandenburgische Technische Universität, Postfach 10 13 44, D-0313, Cottbus, Germany; and 3 Wetland Biogeochemistry Institute, Louisiana State University, Baton Rouge, Louisiana 70803 USA
Received for publication August 10, 1999. Accepted for publication October 29, 1999.
ABSTRACT
The objective of this work was to determine whether radial oxygen loss (ROL) from roots of Typha domingensis and Cladium jamaicense creates an internal oxygen deficiency or, conversely, indicates adequate internal aeration and leakage of excess oxygen to the rhizosphere. Methylene blue in agar was used to visualize the pattern of ROL from roots, and oxidation of a titanium-citrate solution was used to quantify rates of oxygen leakage. Typha's roots had a higher porosity than Cladium's and responded to flooding treatment by increasing cortical air space, particularly near the root tips. A greater oxygen release, which occurred along the subapical root axis, and an increase in rhizosphere redox potential (Eh) over time were associated with the well-developed aerenchyma system in Typha. Typha roots, regardless of oxygen release pattern, showed low or undetectable alcohol dehydrogenase (ADH) activity or ethanol concentrations, indicating that ROL did not cause internal deficiencies. Cladium roots also released oxygen, but this loss primarily occurred at the root tips and was accompanied by increased root ADH activity and ethanol concentrations. These results support the hypothesis that oxygen release by Cladium is accompanied by internal deficiencies of oxygen sufficient to stimulate alcoholic fermentation and helps explain Cladium's lesser flood tolerance in comparison with Typha.
Key Words: alcohol dehydrogenase • cattail • Cladium • Cyperaceae • ethanol • Everglades • flood tolerance • redox potential • root oxygen • sawgrass • Typha • Typhaceae
For a plant growing in a flooded soil, a major stress is the lack of an external oxygen supply to support aerobic root respiration. A common strategy exhibited by wetland plants is internal aeration accomplished through the development of aerenchyma or air-space tissue, which provides a continuous, intercellular pathway for the rapid flux of oxygen through tissues growing in an anaerobic soil (Armstrong, 1979
). The most successful wetland species exhibit modified root morphology and anatomy to accommodate internal oxygen movement from the shoot to the growing root tips (Armstrong, Brändle, and Jackson, 1994
). Diffusion of oxygen through plant roots is complicated, however, by the occurrence of respiration (internal oxygen sink), internal barriers to diffusion (tortuosity), and leakage of oxygen along the diffusional pathway to the surrounding soil, the latter being influenced by root permeability and sediment oxygen demand (external oxygen sink) (Armstrong et al., 1991
; Sorrell and Armstrong, 1994
)
Rhizosphere oxidation resulting from radial oxygen loss (ROL) from plant roots has also been touted as an important adaptation that helps buffer flood-tolerant plants against toxic, reduced compounds that accumulate in anaerobic soils (Armstrong, 1979
; Grosse and Schroder, 1985
; Carpenter and Lodge, 1986
; Jaynes and Carpenter, 1986
; McKee, Mendelssohn, and Hester, 1988
). ROL and the development of an oxidized rhizosphere would only be a useful strategy, however, if this process does not significantly deplete internal oxygen supplies. If high rates of ROL interfere with the maintenance of internal oxygen concentrations, aerobic respiration might be significantly inhibited at growing tips.
Specific anatomical and morphological characteristics are correlated with patterns of ROL and suggest that control of oxygen losses to the surrounding soil is important to maintenance of internal supplies. A number of wetland species apparently restrict ROL (Armstrong, 1971
) through the development of a rhizodermal barrier to diffusion in the differentiated portions of their roots and rhizomes. In contrast, many nonwetland species exhibit ROL along the entire root length. Thus, one distinguishing characteristic of flood-tolerant and intolerant species is in their different patterns of oxygen loss along the root axis (Armstrong, 1971
). Greater oxygen release from younger roots and those bearing fine laterals (Sorrell, 1994
) further demonstrates how differences in root systems can influence ROL patterns and rates.
A few workers have suggested a competition for oxygen between root cells and the rhizosphere (Koncalova', 1990
; Armstrong et al., 1991
), and examination of ROL and ethanol concentrations in rice roots provided some evidence for a relationship between these oxygen sinks (Waters, Armstrong, and Thompson, 1989
). If ROL leads to decreases in internal oxygen supplies, aerobic respiration may be inhibited. Plant roots can metabolize anaerobically for short periods when internal aeration is insufficient to maintain aerobic respiration. However, lack of oxygen is ultimately lethal to active root meristems (Xia and Saglio, 1992
). In addition, net energy production by anaerobic pathways is only a fraction of that produced by aerobic respiration, and carbon consumption may be accelerated to meet minimum energy requirements (Crawford, 1992
). Even highly flood-tolerant species may exhibit oxygen deficiencies, stimulation of alcoholic fermentation, and decreased energy status in their roots when conditions exceed tolerance limits (Mendelssohn, McKee, and Patrick, 1981
; McKee and Mendelssohn, 1987
; McKee, Mendelssohn, and Burdick, 1989
). The decrease in energy status caused by excessive flooding affects root growth directly, but it also has a negative impact on nutrient uptake and shoot growth (Koch, Mendelssohn, and McKee, 1990
).
We hypothesize that roots exhibiting high rates of oxygen efflux will have high activities of alcohol dehydrogenase (ADH), the terminal enzyme in alcoholic fermentation, because oxygen that is needed inside the root is lost to the rooting medium, and internal deficiencies develop. Alternatively, roots with high oxygen efflux will show low ADH activity because the roots are receiving so much oxygen that the amount lost to the rhizosphere is insignificant in comparison to that delivered to respiring cells in the root.
We also hypothesize that the relationship between root oxygen loss and internal aeration differs among wetland plant species. Species may differ greatly in their inherent tolerance of stressors such as flooding and are often arrayed along an elevational gradient accordingly (Crawford, 1987
). When conditions are changed by natural or anthropogenic events, however, the relative success of species in a particular habitat may be altered. One such case occurs in the Florida Everglades where the natural dominant, Cladium jamaicense Crantz. (sawgrass), is gradually being replaced in some areas by Typha domingensis Pers. (cattail) (Urban, Davis, and Aumen, 1993
; Davis, 1994
). Although the causes for the conversion of sawgrass to cattail stands are complex, several investigations have pointed to two major factors: increased phosphorus loading from adjacent agricultural areas (Koch and Reddy, 1992
; Urban, Davis, and Aumen, 1993
; Davis, 1994
; Newman, Grace, and Koebel, 1996
; Miao and Sklar, 1998
; Newman, Schuette and Pietrucha, 1998
) and extended hydroperiod (Loveless, 1959
; Herndon, Gunderson, and Stenberg, 1991
; Urban, Davis, and Aumen, 1993
; Light and Dineen, 1994
; Busch, Loftus, and Oron, 1998
). Studies suggest that Typha is highly flood tolerant, whereas Cladium is more sensitive to extended periods of flooding or low redox potential (Grace, 1989
; Herndon, Gunderson, and Stenberg, 1991
; Urban, Davis, and Aumen, 1993
; Newman, Grace, and Koebel, 1996
; Pezeshki et al., 1996
; Kludze and Delaune, 1996
). Thus, our second objective was to determine whether Typha and Cladium differ in their root anatomy, root oxygen loss rate or pattern, and relative ability to maintain internal aeration of roots growing in anaerobic or reducing media.
MATERIALS AND METHODS
Plant material and experimental design
Seeds of Typha and Cladium were collected from the oligotrophic area of Water Conservation Area 2A (WCA 2A) in the northern Everglades and germinated on moist filter paper in petri dishes ([in a growth cabinet under alternating thermoperiod (25/10°C day/night) and photoperiod (14 h day)]). Seedlings (5–6 wk old) were established in separate containers of commercial potting soil amended with macronutrients to support optimal growth (Jiffy-Mix Plus, Jiffy Products of America, West Chicago, Illinois, USA) under drained (but moist) and constantly flooded (5 cm above soil surface) treatments and maintained in the greenhouse for 55 d. Plants were watered daily to replace losses due to evapotranspiration. At the end of this period when the plants were ~40 cm tall, roots from both treatments were rinsed of soil with tap water, followed by deionized water, and used for measuring ROL rates, porosity, anatomy, and enzyme activity as described below.
A second set of plants was established in hydroponic culture to facilitate the rhizosphere oxidation measurements (25% strength modified Hoagland's nutrient solution, which provided nitrogen as NH4Cl [5 mg/L] and phosphorus as KH2PO4 [7.75 mg/L]) (Hoagland and Arnon, 1950
). After 6–10 wk in a greenhouse with midday light intensity of 1500 µmol·m-2·s-1 photosynthetic photon flux density (PPFD), these plants were used to visualize rhizosphere oxidation patterns in methylene-blue agar as described below. Porosity, ADH activity, and ethanol accumulation were measured in roots exhibiting different oxidation patterns.
All roots were either stored moist and on ice in plastic bags (porosity and anatomy) or in liquid nitrogen (enzyme) until analysis.
Root porosity
Roots from hydroponic and soil cultures were examined for porosity by the pycnometer method (Jensen et al., 1969
). Representative fresh roots (15–30 cm long) were removed intact, and subsections from two locations were excised: 5 cm from the root tip (hereafter referred to as apical) and 5 cm from the root base (hereafter referred to as basal). Three determinations per root subsection per treatment were made.
The specific gravity (SG) was determined using 0.2–0.4 g of root tissue and a 25-mL pycnometer. The roots (R), the water-filled pycnometer (W), and the roots within the water-filled pycnometer (PR) were weighed, and the formula SG = R/(W + R - PR) yielded specific gravity. These roots were retrieved from the pycnometer, ground into a paste with mortar and pestle, and the homogenate was returned to the pycnometer for reweighing. Root porosity was determined using the formula: POR = (PG - PR)/(W + R - PR) x 100, where the symbols are as above, POR = porosity in percent and PG = mass of pycnometer with ground roots and water. An estimate of cross-sectional air space was calculated by multiplying root cross-sectional area by porosity.
Root anatomy
Free-hand, transverse sections of roots from drained and flooded soil cultures were made on fresh tissue that was kept moist in dampened blotting paper. A representative root segment (10–25 cm long) was divided into four parts (apex, 2 cm proximal to apex, base, and 3–4 cm distal to base). Sections were stained with toluidine blue (0.05%) and examined for aerenchyma formation and cell wall thickness.
Root ADH activity and ethanol
ADH activity and ethanol were measured in the roots of Typha and Cladium as indicators of root oxygen deficiency (Mendelssohn and McKee, 1987, 1992
). Roots from plants grown under flooded and drained soil cultures and from the methylene-blue agar (hydroponic) analysis were used. In the latter case, the roots were subdivided into those showing ROL and those showing no or minimal ROL. For extraction and assay of ADH, root tissue (~0.50 g fresh mass) was homogenized with a Brinkman Polytron homogenizer in 5 mL of 50 mmol/L HEPES buffer (pH 7.3), which contained 2 mmol/L cysteine-HCL, 5 mmol/L MgCl2, and 2% (w/v) PVPP (polyvinyl-polypyrrolidone) and vortexed for ~15 s. The plants extracts were centrifuged at 12 000 rpm for 15 min at 4°C. A subsample was prepared and analyzed for ADH activity at 30°C as follows: 0.1 mL of extract was added to a reaction cuvette containing 1 mL assay buffer (39 mmol/L HEPES, 5 mmol/L MgCl-H2O), 0.1 mL of 0.26 mmol/L NADH, and 0.1 mL of 0.40 mmol/L acetaldehyde and read against a reference cell containing all components except acetaldehyde. The rate of NADH oxidation was followed for 3–5 min on a spectrophotometer at 340 nm. Ethanol determination was performed enzymatically on the extract by measuring the reduction of NAD. A 300-µL aliquot was added to a vial containing NAD-ADH (commercial kit, Sigma Company, St. Louis, Missouri, USA) in 3 mL of glycine buffer, incubated at 30°C for 10 min, and the absorbance was read at 340 nm against a glycine buffer blank.
Radial oxygen loss from roots
The rate of oxygen release from Typha and Cladium roots grown in soil was estimated colorimetrically with a Ti+3-citrate solution as described previously (Sorrell, Brix, and Ott, 1993
). Ti+3-citrate was prepared under an N2 atmosphere according to the method of Zehnder and Wuhrmann (1976)
. The plants from both drained and flooded treatments were extracted from the pots, and their roots were carefully washed in tap water to remove all soil and rinsed in deionized water. The intact root systems were then gently blotted on tissue paper and immersed (one plant per flask) in 200 mL of 25% strength Hoagland's solution containing Ti+3-citrate. Six hours after immersion, absorbance of the partially oxidized Ti+3-citrate solution was read at 527 nm on a spectrophotometer. Released oxygen was calculated with the formula
 |
Oxygen release patterns
Patterns of oxygen leakage from Typha and Cladium roots grown hydroponically were examined (four replicates per species) using the methylene-blue agar method described by Trolldenier (1988)
. A solution containing 0.2% agarose and 1 mmol/L CaCl2 was prepared by heating (not more than 70°C). The mixture was cooled to 40°C, and methylene blue (10 mg/L) was added. This solution was then reduced using 0.6 g/L sodium dithionite (Na2S2O4) and gently shaken until it was colorless. The solution was transferred to clear acrylic viewing boxes (20 x 20 x 1 cm) and purged with nitrogen gas to prevent oxidation of leuco-methylene blue.
When the methylene-blue agar solution cooled to 25°C, Typha or Cladium roots were immersed in the liquid in the viewing boxes. The surface of the agar was immediately covered with a 2.5 cm deep layer of paraffin oil to avoid direct contamination with atmospheric oxygen. The part of the plant shoot in contact with paraffin oil was protected by a layer of parafilm. The entire experimental unit was transferred to a growth chamber where changes in color and redox potential of the agar solution were monitored over a 6-h period.
Oxidation of the methylene blue, as indicated by a blue halo formation, and changes in redox potential were recorded systematically every 10 min over a 70-min period. Photographs of halo formation around roots were taken at 60 min. Bright platinum electrodes were inserted alongside selected primary roots (within blue haloes) and into the adjacent bulk agar to measure redox potential (Eh). Eh was calculated by adding the potential of the calomel reference electrode (+244 mV) to the millivolt (mV) reading. Samples of agar inside halos were extracted with a syringe and frozen for later analysis of ethanol. The roots were gently extracted from the agar after removal of the paraffin oil, rinsed with deionized water, and partitioned into groups with and without oxidation halos. These roots were analyzed as described above for porosity, anatomy, enzyme activity, and ethanol.
RESULTS
Root porosity
In both Typha and Cladium, root porosity varied between 10 and 30%, depending on flooding treatment and root segment examined (Fig. 1). Porosity was lower in Cladium roots overall (P < 0.0001), but flooding caused both species to increase root air space (P < 0.0001) (Table 1). A significant interaction between species and treatment (P < 0.0001) for apical porosity indicated that Typha responded more than Cladium to flooding treatment with increased air space development near root tips (Fig. 1, Table 1).
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Root ADH activity and ethanol
Recovery of internal standards added to root extracts from both species and all treatments was high (75–100%; N = 24), indicating the adequacy of the extraction and assay methods employed and minimal interference by plant secondary compounds. Significant main effects of species and treatment on ADH (P < 0.0001 and P = 0.0001, respectively) and ethanol (P < 0.0001 and P = 0.0048, respectively) showed that the capacity for alcoholic fermentation was higher overall in Cladium roots and that both species likely responded to flooding by increasing alcoholic fermentation (Fig. 3). A significant interaction effect on ADH (P = 0.0724) and ethanol (P = 0.0226), however, showed that the response by Cladium to flooding was greater than that of Typha.
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A number of studies have demonstrated oxygen release from the roots of plants (Armstrong, 1971
; Beckett et al., 1988
; Brix, Sorrell, and Orr, 1992
; Engelaar, Van Bruggen, and Van Den Hoek, 1993
; Sorrell and Armstrong, 1994
) and illustrated the key role this process may play in preventing excessive exposure to phytotoxins (Ponnamperuma, 1972
; McKee, Mendelssohn, and Burdick, 1988
; Chabbi et al., 1998
). ROL, however, may exact a cost to the plant by decreasing internal supplies of oxygen sufficiently to affect aerobic respiration. Our results demonstrate that Typha exhibits ROL along the subapical root axis, and this pattern actually reflects an oxygen supply in excess of that needed to meet internal demands. Cladium is less efficient in internal aeration and must restrict oxygen losses by developing barriers to ROL along most of the root axis. The fact that Cladium roots exhibited increased ADH activity and ethanol concentrations when waterlogged or exposed to strongly reducing conditions further suggests that the restriction of ROL to the root apex does not ensure avoidance of oxygen deficiencies when external oxygen demand is high.
The differences between Typha and Cladium in terms of ROL patterns and metabolic response were consistent with their respective root anatomies. Both species' roots were characterized by an aerenchymatous cortex, which facilitates internal gas transport in tissues growing in an hypoxic or anoxic environment (Armstrong, Brändle, and Jackson, 1994
). Soil waterlogging may induce greater root porosity in some wetland species (Burdick, 1989
), and both Typha and Cladium responded to flooding treatment by increasing air-space development to some extent. Porosity of Cladium's roots, however, was somewhat lower than Typha's and showed smaller changes in response to flooding (Fig. 1, Table 1). The greater response by Typha suggests that its strategy is to maintain low resistance to oxygen flux in its roots. Cladium exhibited another strategy, involving limitation of oxygen losses from the roots through the development of barriers to leakage along the root axes (Figs. 2E, 6B). Root sections showed thickening of hypodermal cell walls in differentiated regions distal to the root apex (Fig. 2E), as found for other wetland macrophytes (Sorrell, 1994
). Restriction of ROL to the apical region has been reported for other species and assumed to indicate an efficient aeration system (e.g., Smits et al., 1990
; Chabbi et al., 1998
). This ROL pattern was in fact correlated with a lower overall ROL rate, indicating lower losses to external sinks by Cladium.
What are the consequences of these different rates and patterns of oxygen release for the metabolic activity of Typha and Cladium roots? We specifically tested the assumption that oxygen leakage from roots would interfere with internal aeration by examining ADH activity and ethanol concentrations. ADH is the adaptive enzyme that catalyzes the reduction of acetaldehyde to ethanol during alcoholic fermentation (Crawford, 1967
; John and Greenway, 1976
), and its activity has been used as an indicator of root oxygen deficiencies and waterlogging stress for many wetland plants (Smith and Ap Rees, 1979
; Mendelssohn, McKee, and Patrick, 1981
; McKee and Mendelssohn, 1987
; Burdick, Mendelssohn, and McKee, 1989
; McKee, Mendelssohn and Burdick, 1989
; Burdick and Mendelssohn, 1990
). High levels of ADH activity and ethanol not only occurred in Cladium roots grown in waterlogged soils (Fig. 3), but measurement of these variables in Cladium roots with and without oxygen release demonstrated that ROL does affect root metabolism when external sinks are strong (Fig. 7). The absence of ethanol in the agar medium surrounding Cladium's roots may have been due to ethanol consumption by the roots, as reported for rice (Waters, Armstrong, and Thompson, 1989
). Alternatively, ethanol could have been consumed by microorganisms attached to the root surface.
The lack of detectable levels of ADH and ethanol in Typha's roots (with and without oxygen release) indicated that even when oxygen loss occurred along the entire root axis, it did not lead to internal deficiencies in this species. Typha's ability to avoid root oxygen deficiencies when subjected to a strongly reduced medium is in contrast to that reported for some other highly flood-tolerant species. Oryza sativa (John, Limpuntana, and Greenway, 1974
) and Spartina alterniflora (Mendelssohn, McKee, and Patrick, 1981
) roots could not sustain complete aerobic metabolism under strongly reducing conditions. The reason for Typha's efficient internal aeration is partly explained by its higher root porosity, but may also be due to the occurrence of convective flow ventilation, a process whereby oxygen is moved by mass flow rapidly through the shoots of some species, dramatically increasing the supply of oxygen to the root system (Beckett et al., 1988
; Brix, Sorrell, and Orr, 1992
; Chanton et al., 1993
; Armstrong, Armstrong, and Beckett, 1996
). Of 14 emergent freshwater macrophytes examined, the highest flow rates were produced by Phragmites australis (Cav.) Trin. ex Steud., Typha orientalis Presl., and T. domingensis (Brix, Sorrell, and Orr, 1992
). Genera such as Typha with a high potential for internal pressurization and low internal resistance to flow are capable of growing in deep water (Brix, Sorrell, and Orr, 1992
). Not all emergent wetland macrophytes exhibit internal pressurization and convective flow, however, and in its absence must depend on gas-phase diffusion (Armstrong, Armstrong, and Beckett, 1996
). This is the case with Cladium, where minimal pressurization (7 Pa) and no flow were measured in plants growing in a Louisiana marsh (Sorrell, Mendelssohn, and McKee, unpublished data). By comparison, T. domingensis and P. australis growing in the same marsh generated significant internal pressures (116 and 376 Pa, respectively) and very high flow rates (6.9 and 4.8 mL·min-1·shoot-1, respectively).
A more efficient ventilation and supply of oxygen to plant roots can lead to greater oxygen flux to the rooting medium (Armstrong, Armstrong, and Beckett, 1996
). ROL and the development of an oxidized rhizosphere would not only buffer roots against soil toxins (McKee, Mendelssohn, and Hester, 1988
), but also influence mineralization rates and form and availability of nutrients in the root zone (Reddy, Patrick, and Lindau, 1989
). Halo formation near Typha and Cladium roots in the agar gels was quantified by monitoring changes in Eh over time and demonstrated that Typha has a much greater capacity to oxidize its rhizosphere than does Cladium (Fig. 6). Eh may have increased in Typha's rhizosphere because of a faster efflux of oxygen relative to the rate of oxygen reduction in the reduced methylene blue. Pressurized ventilation of Typha may be largely responsible for this response, but a lower internal demand for oxygen cannot be ruled out. The oxygen leaking from Cladium roots was sufficient to cause halo formation, but the rate of oxygen leakage from roots apparently equaled the rate of reduction so that no net change in Eh occurred over time (Fig. 6).
In summary, ROL patterns differed for Cladium and Typha; leakage of oxygen along the root axis did not lead to internal deficiencies in Typha, but instead reflected root oxygen supplies in excess of that lost to external and internal sinks. Cladium, which mainly restricted ROL to the root apex, still experienced internal oxygen deficiencies when external oxygen demand was high. These results suggest that Typha has a greater capacity to maintain root and rhizosphere aeration during flooding than does Cladium.
Ecological implications
The results of this study are important to an understanding of the vegetation changes occurring in the Florida Everglades, where areas once dominated by Cladium are being invaded by Typha (Jensen et al., 1995
; Newman, Schuette, and Pietrucha, 1998
). This unique ecosystem, which once included over 1 million ha of contiguous freshwater wetlands, developed in a habitat characterized by low availability of nutrients and periodic fluctuations in water level caused by seasonal and annual variations in rainfall (Davis, 1943
; Steward and Ornes, 1975
). During this past century, portions of the Everglades have been drained and cultivated, whereas others have been enclosed within a series of diked impoundments (water conservation areas) for various purposes including stormwater storage, water supply, recreation, and wetland preservation (Davis, 1989
). As a result, the hydrologic regime and flow patterns have been drastically altered, and runoff from agricultural areas has increased phosphorus and nitrogen loading into the Everglades (Koch and Reddy, 1992
; Newman, Schuette, and Pietrucha, 1998
).
The immense expanse of vegetation forming the Everglades has historically been dominated by Cladium, either in vast, monospecific stands or mixed with a variety of other macrophytes, including Typha (Loveless, 1959
). However, Typha was not a major species in the Everglades before the alterations in hydrology and nutrient regime. Typha has since increased in abundance and now forms monospecific stands in three general types of areas where water depth and duration have increased, agricultural water enters the wetland, and/or vegetation has been physically disturbed (Davis, 1989
; Urban, Davis, and Aumen, 1993
; Jensen et al., 1995
; Newman, Schuette, and Pietrucha, 1998
). This history not only suggests that the physical and chemical changes wrought by human activities have precipitated the vegetative change now occurring there, but that the proximal causes are many and possibly interactive.
The contrasting responses of Cladium and Typha to waterlogged soils and reduced agar gels in our study provide some insights into the mechanisms underlying species differences in flood response. Typha's main strategy is one of avoidance, i.e., it avoids the main effect of waterlogging by maintaining sufficient supplies of oxygen internally and by decreasing the number of respiring cells, thereby decreasing oxygen sinks along the diffusional pathway. Thus, the potential for development of oxygen deficiencies at growing root tips is minimized in this species during flooding, and excess oxygen is released to the rhizosphere where it provides further protection by creating an oxidized buffer zone. These findings agree with the highly flood-tolerant nature of Typha and its ability to grow in relatively deep water for extended periods (Grace, 1989
; Brix, Sorrell, and Orr, 1992
). Furthermore, a recent analysis of factors influencing cattail growth and distribution in the Everglades found that: (1) in the absence of P limitation, cattail abundance was influenced by either fire or hydrology and (2) 46% of the variation in cattail cover at one study site was explained by elevation, suggesting that increased water depth and duration of flooding had a major impact on cattail expansion there (Newman, Schuette and Pietrucha, 1998
).
Cladium, by contrast, simply tolerates flooding and puts less effort into avoidance strategies. It has a lower overall root porosity, and flooding causes only limited increases in air space tissue. Lower porosity not only means that gas transport is slower (Justin and Armstrong, 1987
; Laan, Tosserams, and Blom, 1989
), but also that the proportionally lower volume of oxygen in these air spaces is depleted more quickly by losses to respiration and to external sinks. Thus, Cladium must limit the loss of oxygen to the surrounding medium through the development of barriers to ROL (Armstrong, 1979
; Colmer et al., 1998
; Fig. 2). For Cladium, even though ROL occurs mainly near root tips, losses associated with fine lateral roots may be high, and internal oxygen concentrations may still become low enough during flooding to induce alcoholic fermentation. Also, the limited development of an oxidized rhizosphere would further render this species more vulnerable to soil phytotoxins accumulating in the root zone.
The flooding depth under which Typha and Cladium were compared in this study was relatively low compared to that present in the field. In spite of this, strong differences between species were evident. Thus, reducing soil conditions, even with minimal shoot inundation, will exert different effects on these species' capacity for root and rhizosphere aeration. Even though Typha's ability for root aeration may be decreased when its shoots are inundated to greater depths, Cladium should be even more affected. However, responses of mature vegetation to flooding may be different from that of the young plants used in this study and must be examined to fully understand species differences in flood tolerance.
The different ROL patterns and root metabolic responses exhibited by Typha and Cladium also suggest differences in terms of potential for nutrient acquisition during flooding. Typha is able to maintain a high flux of oxygen to support aerobic metabolism and energy production needed for nutrient uptake and other active processes. Cladium, with its inability to maintain complete aerobic metabolism under extended hydroperiod, would likely suffer a decrease in energy production, which would in turn limit nutrient uptake to some extent (Koch, Mendelssohn, and McKee, 1990
).
An effect of oxygen deficiency on nutrient acquisition raises the possibility for an interaction between flooding and nutrient availability, which directly relates to the current situation in the Everglades. Although our work compared Typha and Cladium grown under nonlimiting nutrient conditions and was focused on mechanisms of flood tolerance, the outcome of species interactions under natural conditions will involve multiple factors and their interactions. In particular, the availability of soil phosphorus and other nutrients may directly affect species' relative growth responses (Urban, Davis, and Aumen, 1993
; Newman, Grace, and Koebel, 1996
) or indirectly through changes in sediment oxygen demand caused by nutrient inputs (Belanger, Richards, and Walton, 1989
). Flooding may also interact with nutrient availability to influence root production and/or root morphology, which in turn affect both root aeration and nutrient acquisition (e.g., through changes in root surface area). Other factors, such as disturbance, could interact with changes in hydroperiod and fertility to further imbalance competitive interactions between Cladium and invasive species such as Typha.
FOOTNOTES
1 The authors thank J. Lessmann, Q. Lin, P. Geets, N. Kuhn, P. Faulkner, and M. Greiner for laboratory assistance, and S. Miao, F. Sklar, P. V. McCormick, C. Fitz, S. Newman, R. Howard, T. Charron, D. Johnson, and Y. Wu for comments on the manuscript. Professor Hütt of the Lehstuhl für Bodenschutz und Rekultivierung, Brandenburgische Technische Universität Cottbus supported Dr. Chabbi's study leave at Louisiana State University. This research was funded by a contract from the South Florida Water Management District. 
4 Current address: U.S. Geological Survey, National Wetlands Research Center, 700 Cajundome Blvd., Lafayette, Louisiana 70506 USA.
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