Periphyton responses to experimental phosphorus enrichment in a subtropical wetland

Aquatic Botany 71 (2001) 119–139

Periphyton responses to experimental phosphorus enrichment in a subtropical wetland Paul V. McCormick a,∗ , Mary B. O’Dell a , Robert B.E. Shuford III a , John G. Backus a , William C. Kennedy b a

Everglades Systems Research Division, South Florida Water Management District, 3301 Gun Club Road, West Palm Beach, FL 33406, USA b Water Quality Monitoring Division, South Florida Water Management District, 1480-9 Skees Road, West Palm Beach, FL 33411, USA

Received 1 February 2000; received in revised form 24 April 2001; accepted 24 April 2001

Abstract A field experiment was conducted to determine the effects of increased phosphorus (P) loading on periphyton abundance, productivity, and taxonomic composition in an oligotrophic Everglades slough characterized by abundant metaphyton and epiphyton. Mesocosm enclosures were dosed weekly with different orthophosphate loads (0–12.8 g P m−2 per year) for 5 months during the summer wet season (late June–November 1995). Added P was accumulated rapidly by the periphyton at a rate proportional to the load. Phosphorus accumulation caused the loss of the extensive mats of cyanobacteria and diatoms that were abundant in the surrounding slough. This oligotrophic assemblage was replaced by floating mats of eutrophic cyanobacteria and diatoms at the highest loading rates (6.4–12.8 g P m−2 per year), and by diffuse masses of filamentous chlorophytes at intermediate loads (1.6–3.2 g P m−2 per year). Metaphyton and epiphyton biomass-specific productivity increased in proportion to the loading rate and remained elevated at higher loads until the end of the wet season. Respiration rates also tended to increase with P load but were never significantly higher than in unenriched mesocosms. Despite higher productivity rates, both epiphyton biomass and floating mat coverage declined at higher loads compared to controls. Periphyton changes induced by P enrichment may affect wetland function by reducing (1) periphyton dominance, (2) the food quality of the periphyton for herbivores, and (3) the nutrient storage capacity of the wetland. Many of these changes also have been documented in other wetlands, thereby implicating P as a principal factor affecting wetland periphyton structure and function. © 2001 Elsevier Science B.V. All rights reserved. Keywords: Algae; Eutrophication; Everglades; Nutrients; Periphyton; Phosphorus; Productivity; Wetlands

∗

Corresponding author. Present address: The Nature Conservancy, 303 Pine Street, Suite 101, Klamath Falls, OR 97601, USA. Tel.: +1-541-273-0789; fax: +1-541-273-8045. E-mail address: [email protected] (P.V. McCormick). 0304-3770/01/$ – see front matter © 2001 Elsevier Science B.V. All rights reserved. PII: S 0 3 0 4 - 3 7 7 0 ( 0 1 ) 0 0 1 7 5 - 9

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1. Introduction Phosphorus (P) is the principal nutrient limiting algal biomass and growth in most freshwater habitats (Schindler, 1977; Hansson, 1992), and the oversupply of this nutrient from human sources is responsible for the eutrophication of these ecosystems worldwide (Tiessen, 1995). The consequences of cultural eutrophication have been well-documented for lakes and rivers and include excessive primary production, altered nutrient cycles, changes in species composition, and decreased biodiversity (Harper, 1992). Wetlands are recognized widely for their ability to remove P and other nutrients from urban and agricultural runoff (e.g. Howard-Williams, 1985). By contrast, only recently has regulatory attention begun to focus on the ecological impacts caused by these nutrient inputs to wetlands (e.g. USEPA, 1990). The Florida Everglades is an oligotrophic, P-limited wetland that has been exposed to increased P loading in recent decades. Historically, the Everglades received extremely low nutrient inputs primarily from atmospheric deposition. Today, atmospheric inputs are augmented by nutrient-enriched agricultural runoff, which has contributed nearly 50% of the P entering the Everglades in recent decades (SFWMD, 1992). Average background total phosphorus (TP) concentrations in the marsh range between 4 and 10 ␮g l−1 compared with concentrations exceeding 100 ␮g l−1 in areas that have received agricultural runoff for many years (McCormick et al., 1999). This enrichment has produced several ecological changes within the marsh including increased nutrient content of plants and soils (Koch and Reddy, 1992; Miao and Sklar, 1998), increased primary production (Davis, 1989), shifts in plant and animal species composition (Rader and Richardson, 1994; Rutchey and Vilchek, 1994), and accelerated rates of soil accretion and nutrient storage (Craft and Richardson, 1993; Reddy et al., 1993). Attached (i.e. epiphytic) and floating (i.e. metaphytic) periphyton mats are a dominant ecological feature of the oligotrophic Everglades and may provide one of the earliest reliable indicators of marsh eutrophication (Browder et al., 1994; McCormick and Stevenson, 1998). Studies conducted along nutrient gradients within the marsh have found strong correlations between water-column P and periphyton nutrient content, growth rate, and species composition (Swift and Nicholas, 1987; Grimshaw et al., 1993; McCormick et al., 1996). One of the more obvious changes is the loss of the oligotrophic periphyton assemblage, which is composed of calcium-precipitating (calcareous) cyanobacteria and a diagnostic diatom flora (McCormick and O’Dell, 1996). This assemblage accounts for much of the primary production in oligotrophic open-water (slough) habitats, but is absent from areas of the marsh with elevated P (McCormick et al., 1998). Periphyton provides both habitat and a food source for Everglades invertebrates and fish (Browder et al., 1994) and plays key roles in nutrient storage and soil formation (Gleason and Spackman, 1974; McCormick et al., 1998); therefore, changes in periphyton biomass, productivity, and taxonomic composition may affect many other aspects of marsh ecology. An earlier publication (McCormick and O’Dell, 1996) presented experimental data to show that periphyton taxonomic change along nutrient gradients in the Everglades is a direct result of P enrichment. The present paper details functional (e.g. biomass accumulation, productivity, nutrient content) changes associated with this taxonomic shift and the process whereby the oligotrophic periphyton assemblage is replaced by eutrophic assemblages at

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elevated P loads. These findings are compared with those of previous studies to further develop a conceptual model of wetland periphyton responses to P enrichment.

2. Methods 2.1. Experimental location and design Sampling was conducted in Water Conservation Area (WCA) 2A, a diked marsh in the northern Everglades (latitude 26◦ 17 39.15, longitude 80◦ 25 12.16). Runoff from the Everglades Agricultural Area (EAA) is discharged into this marsh through spillways located along a northern levee. These discharges have contributed most of the P load to the marsh in recent decades (Walker, 1995) and produced elevated water-column P concentrations in its northern areas (McCormick et al., 1996). The study was conducted in a typical slough habitat of the marsh interior where P concentrations and macrophyte biomass were low and periphyton biomass was characteristically high. Twenty-four plots were selected that typified vegetation and water depths within the slough. A circular mesocosm (1.2 m high × 1.5 m diameter) constructed from clear, UV-resistant fiberglass (Solar Components Corporation, Manchester, New Hampshire) was installed in 21 of these plots to enclose a 1.8 m2 area. Mesocosms were pushed 10 cm into the sediments and secured to six polyvinyl chloride (PVC) poles sunk to bedrock. Each mesocosm was perforated with 3-cm diameter holes and fitted with a sliding collar, constructed from the same material and perforated with holes in an identical pattern. The collar allowed the mesocosms to be “opened” (i.e. holes of collar and mesocosm aligned) or “closed” (i.e. holes off-set) to permit water exchange as needed. The three remaining plots were delineated by six PVC poles but otherwise left unenclosed. These outside plots were sampled as for mesocosms and compared with unenriched control mesocosms to detect possible enclosure effects. All plots were accessed from fixed walkways to minimize disturbance to the site. No P was added to three of the mesocosms, which served as unenriched controls. Triplicate sets of the remaining mesocosms were enriched at six different P loading rates: 0.4, 0.8, 1.6, 3.2, 6.4, and 12.8 g P m−2 per year. Background loading rates for the marsh have been estimated at approximately 0.1 g P m−2 per year (Walker, 1995), and experimental loading rates were within the range of those experienced in enriched areas of the marsh downstream of canal inflows during the past 2 decades. Mesocosms were dosed weekly with orthophosphate (NaH2 PO4 ) dissolved in approximately 12 l of slough water. This solution was dispersed evenly within each mesocosm using a gravity-feed system (a 2 cm (o.d.) PVC pipe perforated with several small holes) while taking care not to disturb the enclosed vegetation and periphyton mats. Unenriched mesocosms were dosed with slough water in an identical manner to other treatments while unenclosed slough plots were left undisturbed. Mesocosms were closed just prior to dosing and remained closed for approximately 24 h to allow for biological uptake before opening the following day. Water-column chemistry was monitored weekly for the first 3 months of the study and every other week thereafter. Concentrations of TP and soluble reactive phosphorus (SRP) were measured in each plot just before the weekly load was applied to determine ambient conditions. The instantaneous orthophosphate concentration produced in the water-column

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of each mesocosm by the weekly dose was calculated based on the mass of P added, which was constant among weeks, and the volume of water in each mesocosm, which varied weekly with changes in water depth. Total P and SRP measurements were repeated just prior to opening and subtracted from the calculated dose concentration to quantify the extent of P removal by the enclosed community. With the exception of differences in weekly P additions, loading treatments maintained similar background concentrations of other major ions throughout the study period. 2.2. Periphyton sampling Sampling reported here was conducted during the first 5 months of loading, which corresponded to the wet season (June–November). Despite its subtropical location, seasonal fluctuations in environmental conditions strongly influence ecological conditions in the Everglades (Davis and Ogden, 1994). In particular, periphyton growth and biomass are greatest during the wet season (Swift and Nicholas, 1987; McCormick et al., 1998), when temperature and light are highest. 2.2.1. Periphyton nutrient content When available in sufficient quantities, metaphyton was sampled from each plot twice during the first month and monthly thereafter for nutrient analyses. Five pieces of floating material of roughly equal size were collected by hand from each plot, combined into a common collecting bag, and frozen for later determination of N and P content. Thawed samples were dried at 85–90◦ C for 48–72 h, ground, and then assayed for total nitrogen (TN) using a Carlo-Erba NA 1500 CNS analyzer (Haak–Buchler Instruments, Saddlebrook, NJ) and for TP using a standard perchloric acid digestion (USEPA, 1983). Nutrient content was reported per unit dry mass. 2.2.2. Periphyton metabolism Metaphyton productivity and respiration were measured using material collected from free-floating mats, and epiphyton metabolism was measured using periphyton growing on acrylic dowels (7.5 cm length × 1.0 cm diameter) suspended just below the water surface from a floating rack placed in each plot. These cylindrical artificial substrata were used to avoid clipping macrophyte stems, which could complicate macrophyte measurements being performed in the plots. Preliminary data showed no difference in biomass-specific metabolism between periphyton growing on these artificial substrata and that attached to slough macrophytes (Eleocharis, Nymphaea) (McCormick et al., 1998). Dowel racks were deployed approximately 6 weeks prior to loading to allow for the establishment of the indigenous periphyton assemblage. Gross primary productivity (GPP) and respiration of metaphyton and epiphyton were determined by measuring changes in dissolved oxygen in BOD bottles incubated in situ using methods similar to McCormick et al. (1998). Metaphyton and epiphyton incubations were conducted on alternating weeks between weeks 2 and 15 until no dowels remained on the racks, and metaphyton incubations were continued thereafter on a monthly basis. When present, two metaphyton samples (each approximately 10 g wet weight) were collected by hand from each plot and placed in a light and dark bottle filled with unfiltered,

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ambient slough water. Similarly, epiphyton incubations were conducted by collecting two periphyton-covered dowels from each plot and placing them in a light and dark bottle. Bottles were incubated just below the water surface in the surrounding slough for 1–2 h to achieve similar cumulative irradiance for light bottles on different incubation dates. This method yielded metabolism estimates similar to those of other investigators (e.g. Grimshaw et al., 1997). Irradiance was measured using a LI-1000 datalogger attached to a LI-193SA spherical sensor (LI-COR, Lincoln, NE), which was secured at the same depth as the bottles. Initial and final oxygen concentrations were measured using an air-calibrated polarographic oxygen probe (Orion Instruments, Boston, MA). The incubation time and irradiance (mol photons m−2 ) received by each light bottle were recorded. Triplicate light and dark bottles containing water but no sample were incubated simultaneously to correct for water-column activity, which was always quite low. Periphyton in each bottle was filtered (after scraping material from the dowels) onto a pre-ashed, pre-weighed Whatman GF/C glass fiber filter (1.2 mm pore size), dried at 70◦ C to determine sample dry mass, and ashed at 500◦ C for 1 h to determine ash-free dry mass (AFDM). Periphyton respiration and GPP were calculated and corrected for water-column activity as described by McCormick et al. (1998). Productivity rates were expressed as oxygen evolution per unit biomass (AFDM) per unit irradiance (mol photons m−2 ), while respiration rates were expressed as oxygen consumption per unit biomass per unit time. 2.2.3. Periphyton biomass and growth Abundance and growth of epiphyton and metaphyton were estimated using non-destructive techniques. Acrylic plates (15 cm × 7.5 cm) were suspended just below the water surface in each plot just prior to loading. Two plates were collected from each plot every 2 weeks for the first 3 months of loading and monthly thereafter. Accumulated biomass was scraped from each plate, processed for AFDM as described above for metabolism samples, and normalized for the surface area scraped. Overhead photographs of each plot were taken on eight dates to document changes in the areal coverage of the floating metaphyton. Percent coverage of the four slough cover types (open water, metaphyton—Utricularia purpurea, Nymphaea odorata, Eleocharis cellulosa) was determined by overlaying each 25 cm × 20 cm image with a grid of dots and tallying the number of dots overlying each cover type. Approximately 300–400 grid points on each image were tallied to determine coverage percentages. 2.2.4. Taxonomic composition Five samples of metaphyton were collected from each plot and combined into a single sample every 2 weeks for the first 3 months and monthly thereafter. Samples were processed to determine percent biovolume of the three dominant periphyton groups (cyanobacteria, diatoms, and chlorophytes) using the methods described by McCormick and O’Dell (1996). 2.3. Data analysis Statistical analyses were conducted using SAS, version 6.08. Data were log-transformed as necessary to improve normality and homogeneity of variance among treatments. A t-test was used to detect significant (P < 0.05) differences in response variables between

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unenclosed plots and unenriched mesocosms for each sampling date. Significant effects of P loading on each date were detected using Dunnett’s multiple comparison test, which compared each enriched treatment to the unenriched mesocosms. This test was considered to be conservative as the experiment-wise error rate was fixed at P = 0.05 to reduce the probability of a type I error. These daily comparisons were performed in lieu of repeated-measures ANOVA as assumptions of homogeneity of variance could not be met across treatments and dates for all parameters.

3. Results 3.1. Comparisons between unenriched mesocosms and unenclosed plots Water-column TP concentrations were similar in unenriched mesocosms (mean of 6 ␮g l−1 ) and in unenclosed plots (mean of 5 ␮g l−1 ) throughout the study period. Metaphyton P content also was similar between these control treatments and was consistently <0.2 g kg−1 dry mass (Fig. 1). The ratio of N:P in the metaphyton also was similar between control treatments and ranged between 40:1 and 110:1 (w/w) in individual samples. Rates of GPP were similar for metaphyton (Fig. 1, 0.22 and 3.2 mg O2 g−1 AFDM per unit light) and epiphyton (not shown, 0.78 and 3.26), and did not differ between mesocosms and unenclosed plots. Respiration rates for metaphyton (0.01–7.55 mg O2 g−1 AFDM h−1 ) and epiphyton (0.37–2.16) also were similar between the two treatments and were less than GPP for most samples. Despite similar metabolic rates, biomass accumulated faster on plates in unenclosed plots, although the shape of the accumulation curve was similar between the two treatments (Fig. 1). Underwater light measurements and comparison of GPP rates indicated no difference in the light regime between these treatments, and differences in accumulation rates might be related to reduced water flow in the mesocosms. Metaphyton coverage (Fig. 1) in both treatments ranged between 71 and 81% at the beginning of the experiment and decreased to between 11 and 63% by the end of the wet season, a trend that reflected a normal seasonal decline for this wetland (Swift and Nicholas, 1987). Water lily leaves covered between 1 and 30% of the water surface, and this coverage also declined towards the end of the wet season. Open water accounted for the remainder of the coverage and replaced metaphyton as the dominant category in some plots by the end of the wet season. Three algal groups (cyanobacteria, diatoms (Bacillariophyta), green algae (Chlorophyta)) accounted for nearly 100% of biovolume in all metaphyton samples collected during the experiment. Metaphyton in unenriched mesocosms and unenclosed plots were composed predominantly of cyanobacteria and diatoms in varying proportions throughout the study period, and no significant differences in taxonomic composition were detected between these two treatments (Fig. 2). Filamentous cyanobacteria (e.g. Schizothrix calcicola and Scytonema hofmannii) and the diatoms Mastogloia smithii, Amphora lineolata, and Anomoeoneis serians formed most of this assemblage and accounted for between 25 and 90% of total biovolume in individual samples. Chlorophytes rarely accounted for >10% of metaphyton biovolume and consisted largely of the filamentous taxon Mougeotia.

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Fig. 1. Comparison of periphyton P concentrations, productivity, and abundance between unenriched mesocosms (䊉) and unenclosed plots in the surrounding slough (䊊) during the study period. Points are means of three replicates (except where noted by a replicate number in parentheses for unenclosed plots) ± 1 S.E. Asterisks show statistically significant differences (P < 0.05, t-test) between treatments. Irradiance units are mol photons m−2 .

3.2. Periphyton changes in response to P enrichment 3.2.1. Phosphorus removal and periphyton nutrient content While weekly P loads (i.e. the mass of P added) were constant for each treatment, the water-column SRP concentration produced within the mesocosms by these weekly doses (Table 1) varied with water depth (Fig. 3). Removal of SRP generally was complete in all loads during the first 7-week of dosing, but declined thereafter in the two highest loads to as low as 70% removal (Table 1). A portion of the added SRP remained in the water-column in other P fractions as evidenced by an increase in water-column TP during the 2-h-period following dosing when the mesocosms remained closed. The percentage of P remaining in

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Fig. 2. Percent biovolume of cyanobacteria (grey), diatoms (white), and chlorophytes (black) in unenriched mesocosms and in unenclosed plots in the surrounding slough. Periphyton composition was never significantly different between these treatments.

the water-column as TP varied considerably among mesocosms and weeks but averaged <25% (Table 1). Some of this variation, particularly at low loading rates, was attributed to background fluctuations in TP concentrations and reduced analytical precision near the detection limits for P (4 ␮g l−1 ) rather than to actual changes in removal efficiency. Metaphyton accumulated added P rapidly and generally in proportion to the loading rate (Fig. 4). Metaphyton exposed to the three highest loads (3.2–12.8 g P m−2 per year) accumulated P to concentrations significantly higher than those in unenriched mesocosms within the first 4 weeks of dosing and continued to increase relative to controls for the remainder of the study period (Fig. 4). Metaphyton exposed to loads of 0.8–1.6 g P m−2 per year exhibited a similar accumulation pattern by the end of the wet season, while the Table 1 Median values (range in parentheses) for the weekly pulse of soluble reactive phosphorus (SRP) produced by dosing, the percent of this SRP removed, and the percent of the added phosphorus remaining as total phosphorus (TP) in the water-column Loading rate (g P m−2 per year)

SRP pulse (␮g L−1 )

SRP removal (%)

TP remaining in water-column (%)

0.4 0.8 1.6 3.2 6.4 12.8

11 (7–23) 22 (14–46) 45 (28–91) 88 (57–170) 179 (114–383) 338 (225–586)

100 (84–100) 100 (79–100) 100 (86–100) 100 (80–100) 100 (71–100) 98 (68–100)

25 (0–100) 21 (0–90) 17 (0–53) 18 (0–41) 11 (0–45) 14 (0–42)

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Fig. 3. Fluctuations in water depth during the study period. Water-column concentrations produced by weekly doses (see Table 1) were inversely related to water depth (see text for details).

P content of that at the lowest load (0.4 g P m−2 per year) was never elevated significantly above that in unenriched mesocosms. The N:P ratio of periphyton (not shown) declined significantly at loads ≥0.8 g P m−2 per year compared with unenriched mesocosms after 4 weeks of enrichment, and was significantly lower in all enriched treatments by the end of the study period. Periphyton N:P

Fig. 4. Metaphyton P content in enriched (䊊) and unenriched mesocosms (䊉). Loading rates (g P m−2 per year) are shown in the upper left-hand corner of each graph. Points are means of three replicates (except where noted by a replicate number in parentheses for enriched treatments) ± 1 S.E. Asterisks show statistically significant differences (P < 0.05, Dunnett’s multiple comparison test) between a specific enrichment treatment and unenriched mesocosms.

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ratios at the two highest loads (6.4 and 12.8 g P m−2 per year) declined to 20:1 on a mass basis within 4 weeks, and reached levels near 6:1 at the highest load by the end of the study period. Ratios at lower loads declined more gradually and were ≥11:1 throughout the study period. 3.2.2. Taxonomic composition Statistically significant changes in periphyton taxonomic composition occurred in most treatments at some point during the study period (Fig. 5). Mesocosms exposed to the lowest load (0.4 g P m−2 per year) maintained the oligotrophic cyanobacteria–diatom assemblage found in the surrounding marsh, and the proportional biovolume of the three major taxonomic groups in these treatments never differed significantly from that in unenriched mesocosms. Changes in metaphyton taxonomic composition began occurring at the highest loads (6.4 and 12.8 g P m−2 per year) within the first 4 weeks of dosing and at lower loads (0.8–3.2 g P m−2 per year) during subsequent weeks. These changes included a decrease in the percent biovolume of diatoms and an increase in that of filamentous chlorophytes. The

Fig. 5. Percent biovolume of cyanobacteria (grey), diatoms (white), and chlorophytes (black) in enriched mesocosms. Loading rates (g P m−2 per year) are shown in the upper center of each graph. Asterisks to the right of each bar segment show statistically significant differences (P < 0.05, Dunnett’s multiple comparison test) between a specific enrichment treatment and unenriched mesocosms.

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percent biovolume of cyanobacteria was less sensitive to enrichment, although substantial species shifts occurred within this group with increased P loading. One of the first noticeable effects of P enrichment was the loss of the extensive floating and attached cyanobacteria–diatom mats characteristic of the surrounding marsh. These mats turned from a whitish to a greenish hue and began to disintegrate and slough from associated macrophytes in the two highest loads after just 2-week of dosing. By week 8, this oligotrophic assemblage had disappeared from these treatments, and the mesocosms were largely devoid of either epiphyton or metaphyton. This “clear water” state was followed by the growth of a different cyanobacteria assemblage composed of Chroococcus turgidus, Lyngbya birgei, Oscillatoria princeps, and Plectonema wollei. Filamentous chlorophytes, primarily of the genus Spirogyra, emerged as a secondary component of the periphyton at these two loads towards the end of the season. The relative abundance of diatoms tended to be lower than in the oligotrophic assemblage and the dominant diatom species, including Nitzschia amphibia, Nitzschia filiformis, and Rhopalodia gibba, differed from those in unenriched mesocosms. This assemblage grew primarily as floating mats, which occurred sporadically through time and varied greatly in abundance among mesocosms. The same process of mat disintegration occurred at a load of 3.2 g P m−2 per year, but it was followed by the development of a metaphyton assemblage composed almost exclusively of Spirogyra and lesser amounts of other filamentous chlorophytes. This assemblage

Fig. 6. Metaphyton GPP in enriched (䊊) and unenriched mesocosms (䊉). Loading rates (g P m−2 per year) are shown in the upper left-hand corner of each graph. Points are means of three replicates (except where noted by a replicate number in parentheses for enriched treatments) ± 1 S.E. Asterisks show statistically significant differences (P < 0.05, Dunnett’s multiple comparison test) between a specific enrichment treatment and unenriched mesocosms. Irradiance units are mol photons m−2 .

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formed a diffuse mass that occupied much of the water-column in all mesocosms of this treatment and accounted for as much as 80% of metaphyton biovolume. Diatoms comprised an extremely small portion (<10%) of this assemblage. A similar taxonomic shift began to occur by the end of the wet season at lower loads (0.8 and 1.6 g P m−2 per year) as filamentous chlorophytes became associated with a partially disintegrated oligotrophic mat. 3.2.3. Community metabolism Metaphyton GPP ranged between 0.22 and 13.73 mg O2 g−1 AFDM per unit light across all treatments during the study period and generally increased in proportion to the P loading rate (Fig. 6). Rates of GPP in mesocosms exposed to loads of 0.4–0.8 g P m−2 per year did not differ significantly from controls, whereas GPP at higher loading rates was elevated significantly on several dates. Increased GPP at loading rates of 1.6–12.8 g P m−2 per year during the first few sampling dates was attributable largely to increased metabolism of the pre-existing oligotrophic mat, whereas continued increases at the three highest loads were associated with dramatic changes in taxonomic composition already described. Rates of GPP at these highest loads increased as much as 10-fold relative to unenriched mesocosms by week 16 of dosing (mid-October), but then declined to levels comparable to controls by the end of November (week 22) except at the highest load. Reduced productivity

Fig. 7. Dowel GPP in enriched (䊊) and unenriched mesocosms (䊉). Loading rates (g P m−2 per year) are shown in the upper right-hand corner of each graph. Points are means of three replicates ± 1 S.E. Asterisks show statistically significant differences (P < 0.05, Dunnett’s multiple comparison test) between a specific enrichment treatment and unenriched mesocosms. Irradiance units are mol photons m−2 .

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during these final weeks corresponded with seasonal declines in solar radiation and water temperature. Epiphyton GPP ranged between 0.91 and 11.01 mg O2 g−1 AFDM per unit light across all treatments and also increased with increasing P load (Fig. 7). As with the metaphyton, rates of epiphyton GPP increased significantly at loading rates ≥1.6 g P m−2 per year and averaged two- to three-fold higher than controls. These differences remained relatively constant throughout the measurement period, which ended in early October (week 14) and did not extend into the cooler months as for metaphyton. Periphyton respiration rates (not shown) were highly variable and generally were lower than for GPP. Respiration rates across all loads ranged between 0.01–9.56 and 0.01–4.50 mg O2 g−1 AFDM h−1 for metaphyton and epiphyton, respectively. Although the average respiration rate at the highest load was as much as two-fold greater than in unenriched mesocosms, this increase rarely was significant because of high within-treatment variability. 3.2.4. Biomass accumulation Periphyton biomass (AFDM) on plates accumulated exponentially at all loads and peaked on week 13 (Fig. 8). Maximum biomass was similar for all loads except 3.2 g P m−2 per year, where peak biomass was half of that in unenriched mesocosms. Biomass declined

Fig. 8. Periphyton biomass accumulation on acrylic plates in enriched (䊊) and unenriched mesocosms (䊉). Loading rates (g P m−2 per year) are shown in the upper right-hand corner of each graph. Points are means of three replicates ± 1 S.E. Asterisks show statistically significant differences (P < 0.05, Dunnett’s multiple comparison test) between a specific enrichment treatment and unenriched mesocosms.

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modestly after week 13 at P loads ≤0.8 g P m−2 per year and remained relatively constant for the remainder of the study period. Biomass declines were greater at higher loads and were significant at 3.2 g P m−2 per year following development of an abundant Spirogyra population throughout the water-column. 3.2.5. Metaphyton cover Cyanobacteria–diatom mats and the associated macrophyte Utricularia purpurea covered an average of 76% of the water surface enclosed by mesocosms prior to dosing (Fig. 9). The remaining coverage consisted of floating leaves of Nymphaea odorata (average coverage = 14%) and open water (average coverage = 10%). Average mat cover at loads of 0.4–1.6 g P m−2 per year was generally lower than in unenriched mesocosms, but was never significantly different. Mat cover declined rapidly to an average of <10% of total area at the two highest loads and was reduced significantly below that in unenriched mesocosms by week 9 (Fig. 9). Similar reductions in cover occurred at 3.2 g P m−2 per year and were significant by week 14. Low mat cover was maintained for the remainder of the measurement period at 6.4 and 3.2 g P m−2 per year, whereas mat cover increased in one of the 12.8 g P m−2 per year mesocosms that developed a thick floating mat of the cyanobacterium Plectonema wollei. Declines in mat cover corresponded with an increase in open-water cover at higher P loads (P < 0.05, Dunnett’s multiple comparison

Fig. 9. Percent cover of metaphyton on the water surface in enriched (䊊) and unenriched mesocosms (䊉). Loading rates (g P m−2 per year) are shown in the upper left-hand corner of each graph. Points are means of three replicates ± 1 S.E. Asterisks show statistically significant differences (P < 0.05, Dunnett’s multiple comparison test) between a specific enrichment treatment and unenriched mesocosms.

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test). The cover of water lily never differed significantly among loading treatments during this first season of dosing.

4. Discussion 4.1. Periphyton P status and removal capacity The study site was typical of oligotrophic open-water Everglades habitats, which contain abundant periphyton, low macrophyte biomass, and extremely low water-column P concentrations (<10 ␮g TP l−1 ). Periphyton in these areas is severely P limited as indicated by a low P content (<200 mg kg−1 ) and a high N:P ratio (>100:1 w/w) in this and previous studies (Swift and Nicholas, 1987; Grimshaw et al., 1993; McCormick et al., 1998). These values are at the low end of the range for freshwater periphyton in general (Vymazal, 1995), but are comparable to those in other P-limited wetlands (McDougal et al., 1997; Havens et al., 1999a) and reflect the low loading rates of P to this marsh under natural conditions. The calcareous periphyton exhibited a high capacity for P removal, indicating that this assemblage can contribute to the short-term ability of this wetland to assimilate excess P inputs from agricultural runoff or other human sources. The P content of the calcareous periphyton mats increased rapidly during the initial weeks of dosing at loads between 3.2 and 12.8 g m−2 per year and increased significantly at lower loading rates (0.8–1.6 g m−2 per year) by the end of the measurement period. By contrast, P concentrations of soil, porewater, and plants did not increase significantly in any load during this same period (Newman et al., in press). Studies in oligotrophic wetlands in south Florida (Davis, 1982; Havens et al., 1999a) and elsewhere (Howard-Williams and Allanson, 1981) have found that periphyton mats have a high affinity for P relative to other wetland compartments. In an experimental study similar to ours, Havens et al. (1999a) estimated conservatively that periphyton accumulated at least 40–70% of the P added over a 28-day-period to the water-column of marsh enclosures. Thus, the periphyton assemblage appears to function as a major sink for P in the Everglades interior and, by scavenging excess P, contributes to the maintenance of low P concentrations in water, soils, and macrophytes. 4.2. Loss of the oligotrophic periphyton assemblage in response to P loading The most dramatic and rapid change in the slough community elicited by P enrichment was the loss of the floating and attached calcareous periphyton mats that were abundant under oligotrophic conditions. The P concentration and metabolism of these mats increased in proportion to the loading rate within the first few weeks of dosing. However, disappearance of the mat only occurred at loading rates where internal P concentrations exceeded certain levels, suggesting the existence of a threshold for maintaining mat integrity. At loads of 0.4 g m−2 per year, mat P was maintained at or below 0.20 mg g−1 , a level which was approximately two-fold higher than mats in unenriched mesocosms. Mesocosms receiving this load maintained a periphyton assemblage similar to unenriched mesocosms in terms of taxonomic composition, abundance and productivity. At the three highest loading rates (≥3.2 g P m−2 per year), mat P exceeded 0.20 mg g−1 within 2–3 weeks and

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exceeded 0.25 mg g−1 by week 8. The calcareous mat disintegrated in these treatments within 8–10 weeks and eventually was replaced by periphyton assemblages indicative of enriched conditions. A slower, but similar decline in the calcareous mat occurred at loads of 1.6 and 0.8 g P m−2 per year, where mat P exceeded 0.20 mg g−1 by weeks 18 and 22, respectively. Phosphorus concentrations in calcareous mats sampled from WCA 2A and other Everglades marshes typically range between 0.10 and 0.20 mg g−1 (Swift and Nicholas, 1987; McCormick and O’Dell, 1996), which is consistent with our findings suggesting an upper limit of 0.20 mg g−1 for maintenance of the mat. The GPP of the calcareous mat in enriched mesocosms increased in proportion to mat P concentration and was considerably greater than corresponding increases in mat respiration, indicating that net primary productivity also increased with P loading. Rather than increasing the growth rate and abundance of these mats, however, this stimulatory response was associated with their loss. The decline in mat abundance appeared to result from a loss of physical integrity as the mat began to crumble after only a few weeks of dosing at the highest loads. Mat disintegration may result from chemical or physiological changes that affect the precipitation of calcium carbonate, which forms a rigid coating around the cyanobacteria filaments within periphyton mats in oligotrophic areas (Vaithiyanathan et al., 1997). Although the calcareous mats disappeared prior to the onset of eutrophic metaphyton blooms, the growth of new species on the outer surface of the mat was indicated by the greenish hue of mats undergoing disintegration. Thus, it is possible that P enrichment may stimulate the growth of other algae and bacteria within the mat, and that these species may reduce mat growth and integrity through competition or other inhibitory interactions (e.g. allelopathy, lytic bacteria). More detailed investigations of mat physiology and species-specific growth responses clearly are required to identify the exact mechanism(s) whereby P enrichment causes the loss of the calcareous mat. Abundant cyanobacterial mats occur throughout much of the Everglades interior (Browder et al., 1994), but have not, to our knowledge, been reported in other oligotrophic waters. Areas of the Everglades where these mats flourish clearly are P-limited as TN:TP ratios in the water-column typically exceed 200:1 on a mass basis and both periphyton and vegetation respond preferentially to P enrichment. Experimental studies conducted elsewhere in the Everglades-Lake Okeechobee wetland complex have found these mats to exhibit responses to P enrichment that are similar to those presented here (i.e. rapid P accumulation and increased productivity followed by collapse). In the southern Everglades, these mats were eliminated within 8 weeks in flow-through channels in response to continuous P addition averaging <20 ␮g SRP l−1 (Flora et al., 1988). In the littoral zone of Lake Okeechobee, Havens et al. (1999a) found taxonomically similar mats at background water-column TP of <7 ␮g l−1 and documented the decline of this assemblage within 28 days in response to P loads of 2.8 g m−2 per year. These investigators also found P concentrations in unenriched mats to average <0.20 mg g−1 compared with concentrations near 0.50 mg g−1 in enriched mats undergoing decline. 4.3. Growth of eutrophic assemblages Two distinct periphyton assemblages developed in response to increased P loading. Both were characterized by higher P content, lower N:P ratios, and higher biomass-specific pro-

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ductivity compared to the oligotrophic, calcareous assemblage. However, these eutrophic assemblages also exhibited reduced floating mat cover and lower attached (epiphyton) biomass. Intermediate P loads resulted in a shift in dominance from cyanobacteria to filamentous chlorophytes (e.g. Spirogyra), while the highest loading rates resulted in a shift directly from oligotrophic to eutrophic cyanobacteria (e.g. Plectonema wollei, Oscillatoria princeps). These taxonomic shifts correspond with those documented along marsh nutrient gradients, indicating that changes along these gradients are due largely to P enrichment (McCormick and O’Dell, 1996). Shifts between major taxonomic groups documented here were similar to those in other wetland and shallow-lake enrichment experiments (Howard-Williams, 1981; Hillebrand, 1983; McDougal et al., 1997; Havens et al., 1999b), many of which enriched simultaneously with both N and P rather than with P alone. These similarities suggest that P-limitation is widespread in wetlands and plays an important role in shaping the periphyton assemblage. Differences in dominant species among studies may result from the type of enrichment (e.g. P alone as opposed to N + P), the frequency of addition (e.g. McDougal et al., 1997), and differences in ambient water chemistry conditions other than P among wetlands. Development of a metaphyton-dominated, low-epiphyton system at intermediate loading rates was consistent with current paradigms of periphyton responses to nutrient enrichment in sparsely vegetated wetland habitats (Goldsborough and Robinson, 1996). The filamentous chlorophytes that dominated the periphyton assemblage in these treatments typically exhibit a free-floating growth habitat; however, filaments of these taxa did become entangled around the substrata collected to measure attached biomass, and accounted for most of the “epiphyton” biomass measured in these treatments. Extensive development of this metaphyton assemblage throughout the water-column may have inhibited development of a true epiphyton assemblage through shading and, perhaps, through competition for P and other nutrients (e.g. trace elements such as Fe) that are in low supply in the oligotrophic interior of this marsh. As for the oligotrophic assemblage, the chlorophyte assemblage appeared to be P-limited, as TN:TP ratios on a mass basis averaged well above levels suggestive of N limitation. In an earlier study, Flora et al. (1988) found that additions of P alone or in combination with N resulted in the same shift from cyanobacteria to chlorophytes, providing further evidence that N is not an important limiting Everglades periphyton even under moderately enriched conditions. Cyanobacteria often dominate P-enriched habitats because low N:P ratios favor the growth of N-fixing forms (Schindler, 1977; Smith, 1983). Indeed, development of floating mats of eutrophic cyanobacteria rather than filamentous chlorophytes at the highest P loading rate appear to have resulted from a switch from P to N limitation, as indicated by low N:P ratios of these mats as well as a sharp increase in N content, possibly due to N-fixation activity (Newman et al., in press). Studies conducted along nutrient gradients in this marsh also found this cyanobacteria assemblage in highly enriched areas (water-column TP > 30 ␮g l−1 ) where limiting nutrient assays indicated co-limitation by N and P (McCormick et al., 1996). Despite high nutrient content and high productivity, the biomass of floating and attached mats of the eutrophic cyanobacteria assemblage was low in all but one of the six mesocosms receiving loads of 6.4 and 12.8 g P m−2 per year. Declines in periphyton biomass in response to nutrient enrichment have been attributed to increased phytoplankton biomass

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and consequent inhibition of periphyton growth by shading (Sand-Jensen and Borum, 1991). However, phytoplankton growth never was observed in any treatment in our experiment. Similarly, low periphyton biomass in these treatments could not be explained by competition for light or nutrients with macrophytes as submersed vegetation was absent from these treatments and the cover of floating and emergent vegetation was no greater than in mesocosms receiving lower loads. This same pattern of increased biomass-specific productivity and reduced biomass also has been documented in open-water habitats in enriched areas of this marsh (McCormick et al., 1998). While it is not clear that all the factors contributing to reduced periphyton biomass in enriched mesocosms and in the enriched marsh are the same, these findings do suggest that relationships between wetland nutrient concentrations and algal biomass may be complex and, in some cases, counterintuitive. 4.4. Relevance to ecosystem function and management Periphyton is a major ecological component of the pristine Everglades and changes in the structure and function of this assemblage may affect several other processes in this wetland (Browder et al., 1994; McCormick and Stevenson, 1998). The oligotrophic periphyton assemblage provides an important habitat and food base for Everglades consumers. As shown in other wetlands, shifts towards eutrophic taxa (e.g. filamentous chlorophytes) can reduce the food quality of this resource and its utilization by herbivores (Goldsborough and Robinson, 1996). Calcareous mats also play an important role in soil accretion and are responsible for the formation of marl (i.e. calcium carbonate) soils, which cover large areas of the Everglades (Gleason and Spackman, 1974). Finally, by efficiently scavenging bioavailable P from the water, both through cellular uptake and precipitation of calcium phosphates, this abundant periphyton assemblage likely maintains the extreme oligotrophic conditions that characterize the pristine Everglades. Therefore, loss of the oligotrophic periphyton assemblage provides an early indication that the P assimilative capacity of this wetland has been exceeded and, thus, that ecosystem integrity is being degraded. Wetlands are considered to be effective sinks for added nutrients, and it has been suggested that the ecological integrity of wetland ecosystems (e.g. maintenance of normal community structure and function) can be maintained below some “threshold” P load (e.g. Richardson and Qian, 1999). Our results indicate that short-term ecological changes to P enrichment include both continuous and threshold responses. Physiological changes (e.g. mat P content and GPP) were proportional to increases in P availability. By contrast, shifts in periphyton taxonomic composition (e.g. loss of the oligotrophic assemblage of calcareous cyanobacteria) were rather abrupt and dramatic, and may occur in response to the accumulation of periphyton P above certain critical concentrations. Our results also suggest that ecological responses to P loading are a function of time as well as the absolute loading rate. For example, P accumulation within the periphyton continued throughout the study period and beyond as loading of these mesocosms continued (Newman et al., in press). Thus, assuming that taxonomic changes are in response to excessive P accumulation, it might be predicted that changes observed rather quickly at higher loading rates eventually would occur at lower loading rates. This pattern was observed within

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the timeframe presented here at loads of 0.8 and 1.6 g P m−2 per year, where taxonomic shifts similar to those first observed at 3.2 g P m−2 per year began to occur by the end of the study period. Thus, while the rate of P accumulation and ecological change within the system is determined by the loading rate, the probability that a particular rate will produce ecological change also is a function of the duration of loading (i.e. cumulative load). These findings, while preliminary in nature, do suggest that even relatively small increases in P loading to oligotrophic wetlands such as the Everglades may result in ecological changes over extended time periods as P accumulates within various biological compartments. A more critical assessment of this issue will require longer-term enrichment data.

Acknowledgements The authors thank Eric Smith for assistance with the statistical design and Hunter Carrick, Tom Fontaine, Karl Havens, and Alan Steinman for helpful comments on various drafts of this manuscript.

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