Responses of Seagrass Communities to Fertilization along a Gradient of Relative Availability

of Nitrogen and Phosphorus in a Carbonate Environment

Author(s): Meredith Ferdie and James W. Fourqurean

Source: Limnology and Oceanography, Vol. 49, No. 6 (Nov., 2004), pp. 2082-2094

Published by: American Society of Limnology and Oceanography

Stable URL: http://www.jstor.org/stable/3597513

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Limnol. Oceanogr., 49(6), 2004, 2082-2094 

? 2004, by the American Society of Limnology and Oceanography, Inc. 

Responses of seagrass communities to fertilization along a gradient of relative 

availability of nitrogen and phosphorus in a carbonate environment 

Meredith Ferdiel and James W. Fourqurean2 

Department of Biological Sciences and Southeast Environmental Research Center, Florida International University, Miami, 

Florida 33199 

Abstract 

Patterns of relative nutrient availability in south Florida suggest spatial differences regarding the importance of 

nitrogen (N) and phosphorus (P) to benthic primary producers. We did a 14-month in situ fertilization experiment 

to test predictions of N and P limitation in the subtropical nearshore marine waters of the upper Florida Keys. Six 

sites were divided into two groups (nearshore, offshore) representing the endpoints of an N: P stoichiometric gradient. Twenty-four plots were established at each site with six replicates of each treatment (+N, +P, +N+P, control), 

for a total of 144 experimental plots. The responses of benthic communities to N and P enrichment varied appreciably between nearshore and offshore habitats. Offshore seagrass beds were strongly limited by nitrogen, and 

nearshore beds were affected by nitrogen and phosphorus. Nutrient addition at offshore sites increased the length 

and aboveground standing crop of the two seagrasses, Thalassia testudinum and Syringodium filiforme, and growth 

rates of T. testudinum. Nutrient addition at nearshore sites increased the relative abundance of macroalgae, epiphytes, 

and sediment microalgae. N limitation of seagrass in this carbonate system was clearly demonstrated. However, 

added phosphorus was retained in the system more effectively than N, suggesting that phosphorus might have 

important long-term effects on these benthic communities. The observed species-specific responses to nutrient 

enrichment underscores the need to monitor all primary producers when addressing questions of nutrient limitation 

and eutrophication in seagrass communities. 

The initial response of a coastal ecosystem to eutrophication will be influenced by the status of nutrient limitation 

at the time of enrichment. In coastal marine systems, nitrogen (N) limitation is common in temperate ecosystems with 

siliciclastic sediments, whereas phosphorus (P) limitation is 

often assumed to be restricted to tropical ecosystems with 

carbonate sediments (reviewed by Short 1987; Howarth 

1988). This generalization is largely attributed to biogeochemical sorption processes: strong P affinity to carbonate 

sediments results in a loss of phosphorus available for plant 

uptake. However, not all tropical carbonate benthic ecosystems are P-limited (e.g., Erftemeijer 1994; Udy et al. 1999), 

so there must be other determinants of the limiting nutrient 

in coastal marine ecosystems. 

Confirming the quality (N vs. P or some other element) 

1 Present address: Department of Environmental Sciences, University of Virginia, Charlottesville, Virginia 22903. 

2 Corresponding author (jim.fourqurean@fiu.edu). 

Acknowledgments 

The authors thank Pursell Technologies and IMC Phosphates for 

donating fertilizer used in this study. Joe Boyer and Jennifer Richards served on M.F.'s thesis committee and provided valuable guidance for this project. Tom Frankovich, Cecilia Gordon, Aimee Rotaru, Dottie Byron, and Kevin Cunniff all contributed valuable lab 

and field assistance. Tom Philippi provided valuable guidance on 

the statistical analyses. Two anonymous reviewers provided comments that helped strengthen the paper. 

This study was funded by grant X994620-94-5 awarded to J.W.F 

from the U.S. Environmental Protection Agency as part of the Florida Keys National Marine Sanctuary Water Quality Protection Program and by a Florida International University (FIU) Tropical Biology Program research grant awarded to M.F 

This is contribution 221 of the Southeast Environmental Research 

Center and contribution 74 of the Tropical Biology Program at FIU. 

of nutrient limitation in an ecosystem can be achieved by 

nutrient addition assays, but these assays require relatively 

involved experimental designs, and their interpretation is not 

always clear-cut. In order to generate hypotheses about the 

nature of nutrient limitation, it is possible to examine the 

elemental content of organic matter from ecosystems. The 

elemental content of plant tissue and the ratios of elements 

(i.e., C:N:P) might reflect relative availability and nutrient 

limitation status. Stoichiometry has been used to infer nutrient limitation of phytoplankton (e.g., Redfield 1958), wetland macrophytes (e.g., Bedford et al. 1999), sediment microalgae (e.g., Hillebrand and Sommer 1999), macroalgae 

(e.g., Lyngby et al. 1999), and seagrass (e.g., Atkinson and 

Smith 1983). 

The benthic ecosystem of the Florida Keys are an interesting locale to study nutrient limitation of coastal systems. 

The dominant primary producers in this environment are 

seagrasses and macroalgae, and the water column is transparent and unproductive. Spatial patterns in elemental stoichiometric ratios suggest varying importance of nitrogen and 

phosphorus. Elemental analysis of seagrass (Fourqurean and 

Zieman 2002), water quality (Jones and Boyer 2001), and 

sediment (Szmant and Forrester 1996) display a pattern of 

relatively high N: P nearshore and relatively low N: P offshore toward the Florida Keys Barrier Reef (-10 km from 

the shoreline). On the basis of these stoichiometric patterns, 

it has been hypothesized that the benthic communities in the 

nearshore waters of the Florida Keys are P-limited and offshore waters are N-limited, despite the fact that the entire 

region is underlain with carbonate sediments (Fourqurean 

and Zieman 2002). This implies that benthic community responses to localized nutrient enrichment might differ significantly on the spatial scale of a few kilometers. However, 

2082 
Fertilization of seagrass communities 

nutrient limitation hypotheses derived from stoichiometric 

evidence should be confirmed with nutrient addition assays. 

The classic response of benthic communities to coastal 

marine eutrophication is a shift in vegetation structure from 

slow-growing seagrass and macroalgae to fast-growing microalgae and phytoplankton (e.g., Valiela et al. 1992). This 

sequence is a consequence of interspecific competition and 

changing resource availability. The relative availability of 

resources (e.g., nutrient and light) at a given time will favor 

those species with greater competitive ability for the most 

limiting resource (Tilman 1982). In low-nutrient environments, seagrasses and slow-growing macroalgae are competitive dominants because they have relatively low nutrient 

requirements, can access nutrients in the sediment porewater, 

and possess efficient internal nutrient recycling (see review 

by Duarte 1995). An increase in environmental nutrient 

availability is concomitant with a decrease in light availability to the benthos. Seagrasses have higher light requirements compared with algae because they support metabolism 

for greater belowground biomass. As nutrient availability 

continues to increase, epiphytes and fast-growing macroalgae dominate because they take up nutrients more effectively 

and quickly than seagrass and have relatively lower light 

requirements to sustain growth (e.g., Harlin and ThorneMiller 1981; Twilley et al. 1985). 

Seagrass communities are ideal candidates for nutrient 

limitation studies because they tend to proliferate in shallow 

oligotrophic waters. The seagrass plants themselves are good 

indicators of changes in nutrient regimes because they are 

rooted plants with relatively long lives, they are sensitive to 

changes in water quality, and tissue nutrient content reflects 

the relative availability of nutrients in a system (Atkinson 

and Smith 1983; Duarte 1990). Knowledge of species-specific life history traits and shifts in species dominance might 

also provide insight on changes in nutrient regimes. The 

three most common seagrass species in the Caribbean region 

are Thalassia testudinum, Syringodium filiforme, and Halodule wrightii. From a life history perspective, T. testudinum 

is often dominant in areas of high light and low nutrients. 

S. filiforme and H. wrightii possess faster colonization rates 

and are relatively more efficient at nutrient uptake compared 

with T. testudinum (Williams 1990). We could then predict 

that the relatively slow-growing T. testudinum would be replaced by faster-growing species if nutrient loads were increased. Changes in the distribution and abundance of seagrass, relative to other seagrass species or primary 

producers, could therefore be used to infer changes in the 

nutrient status of a system. 

In this study, we sought to test the hypothesis that seagrass-dominated benthic communities close to shore with 

high N: P ratios are P-limited, whereas those further offshore 

with low N:P are N-limited. We expected that these ecosystems would respond to nutrient enrichment with increasing biomass and productivity. We further expected that additions of nitrogen, phosphorus, or both would alter the N: 

P of the primary producers and that we would see a shift 

from dominance by slow-growing T. testudinum to more rapidly growing primary producers as a consequence of nutrient 

addition. 

Materials and methods 

Study site-The Florida Keys (ca. 250N, 80?S) are a 250- 

km-long archipelago of low-lying islands stretching from 

Key Largo to the Dry Tortugas (Fig. 1). The Keys are 

flanked by the Straits of Florida and Atlantic Ocean to the 

south and east and the Gulf of Mexico and Florida Bay to 

the north and west. South Florida contains the largest continuous seagrass beds in the continental United States and 

some of the most expansive documented seagrass communities in the world (Fourqurean et al. 2002). T. testudinum 

is a common component of the oceanside benthos in the 

Florida Keys. S. filiforme distribution is patchy in the nearshore oceanside areas but increases in density in an offshore 

direction. T. testudinum was selected as a primary response 

species because it is the dominant seagrass species in the 

region and has been identified as nutrient limited in adjacent 

Florida Bay (Powell et al. 1989). 

Experimental design and statistical analyses-A factorial 

nutrient loading experiment was conducted at six sites, divided into two groups that represent the endpoints of the 

stoichiometric gradient: nearshore (<1 km from the shoreline) and offshore (<1 km inside the reef tract). The number 

of replicates for each treatment was determined by a preliminary power analysis. At each site, 24 plots were established 

in a grid (50 X 50 m) with six replicates of each treatment 

(nitrogen addition, +N; phosphorus addition, +P; nitrogen 

and phosphorus addition; +N+P; and control, C). Treatment 

plots (0.5 m2) were evenly spaced within the grid with 10 

m of separation between treatments. 

This experimental design was of the form of a split plot. 

Sites (n = 6) were the (random) whole plots; onshore versus 

offshore were fixed whole-plot "treatments." Quadrats within plots were the subplots (random); nutrient treatments were 

fixed subplot treatments. We treated N and P additions as 

separate factors, with two levels of nitrogen (control, +N) 

and two levels of phosphorus (control, +P). 

Response variables that were only measured at the termination of the experiment were tested with mixed-model 

analyses of variance (PROC MIXED, SAS v9.0), with denominator degrees of freedom calculated via the containment 

method. Nearshore-offshore was tested against sites (1 and 

4 degrees of freedom); nutrient treatments and all interactions between nutrient treatments and nearshore-offshore 

were tested against quadrats (1 and 132 degrees of freedom). 

For response variables sampled repeatedly throughout the 

experiment, sampling dates as categorical repeated measures 

with quadrats within sites as subjects were added to the 

above split plot design. Sampling date was treated as categorical rather than ordered, and error covariances were treated as unstructured rather than autoregressive because of the 

underlying seasonality in many of the measured response 

variables. In order to evaluate differences in environmental 

conditions between onshore and offshore sites, t-tests assuming equal variances were performed on physicochemical and 

sediment parameters. Unless otherwise stated, we deemed a 

comparison statistically significant at p - 0.05. 

2083 
Ferdie and Fourqurean 

Fig. 1. Map of study sites in the upper Florida Keys. 

Nutrient loading rates-Loading rates used in nutrient enrichment experiments ideally must satisfy the following two 

requirements: they must be ecologically relevant, and they 

must be sufficient to ameliorate nutrient limitation. Loading 

rates used in previously published experiments in seagrass 

ecosystems vary widely, and these rates rarely have been 

justified. The use of excessive loading rates in experiments 

is problematic when the goal is to apply experimental results 

to ecological and coastal management applications. To ensure the ecological relevance of this experiment, nutrient 

loading rates were based on regulatory estimates of potential 

maximum wastewater and stormwater discharge (MCSM 

2001), which are the dominant sources of anthropogenic nutrient inputs to the nearshore marine waters of the Florida 

Keys and have been identified as severe threats to regional 

water quality (EPA 1999). Adjustments were made for geochemical (e.g., sorption) and biological (e.g., denitrification) 

processes. A final loading rate of 0.77 g N m-2 d-l and 0.12 

g P m-2 d-l represented a N: P (mole: mole) ratio of 14. The 

rate used in this experiment exceeded the N and P demand 

of T. testudinum during peak growth as assessed by multiplying peak growth rates by nutrient content (Fourqurean et 

al. 1992). 

Fertilizer was added monthly to the sediment. Nitrogen 

was added in the form of urea-coated slow-release N fertilizer (Polyon, Pursell Technologies; 38-0-0, 94% nitrogen as 

urea and phosphorus as deflourinated granular phosphate 

rock [Multifos, IMC Phosphates] Ca3(PO4)2, 18% P). Urea 

is rapidly converted via microbial activity to ammonium 

(Fenchel and Blackburn 1979), which is the dominant form 

of inorganic nitrogen in the coastal waters of the Florida 

Keys (Boyer and Jones 2002). Fertilizer was applied evenly 

to each 0.5-m2 plot and was gently mixed by hand into the 

surface 5 cm of sediment. The sediment surface of control 

plots was also mixed in a similar manner. Fertilizer application near the sediment-water column interface allowed for 

nutrients to diffuse through the sediment porewater and from 

the sediment into the water column, thus exposing both 

above- and belowground macrophyte biomass to nutrient 

manipulations. 

Sampling-The experiment was initiated in May 2001 and 

was terminated in July 2002. Sediment fertilization and collection of abiotic data (light availability, salinity, surface water temperature, turbidity) occurred monthly at each site. 

Light attenuation by the water column was assessed with a 

47r photosynthetically active radiation (PAR) sensor (LICOR, Lincoln, Nebraska). Biotic response variables were 

measured during four major sampling events that occurred 

over the course of 14 months (May 2001, September 2001, 

March 2002, July 2002), in which the first represented a 

prefertilization sampling event. Biomass and nutrient sampling was conducted on those primary producers considered 

most sensitive to changes of nutrient availability in coastal 

marine systems: seagrass, macroalgae, epiphytes, and sediment microalgae. The following response variables were 

measured at all sampling events: T. testudinum leaf productivity, morphology, standing crop, and leaf elemental con2084 
Fertilization of seagrass communities 

tent. At the end of the experiment, we measured sediment 

porosity, bulk density, and organic content, as well as T. 

testudinum rhizome and S. filiforme leaf elemental content; 

S. filiforme leaf length and standing crop; T. testudinum total 

epiphyte load and epiphyte chlorophyll a (Chl a) content; 

sediment microalgae abundance; sediment total N and P content; and nonepiphytic macroalgae abundance. 

At each sampling event, a quadrat (10 X 10 cm) was 

placed inside each treatment plot. T. testudinum growth rates 

were measured on plants within this quadrat by the modified 

hole-punch methodology (Fourqurean et al. 2001). Morphological measurements of all T. testudinum leaves (length and 

width) were recorded, and seagrass standing crop (g m-2), 

areal productivity (g m-2 d-l), and leaf emergence rates of 

marked short shoots (SS) (leaves SS-1 d-1) were calculated. 

The number of S. filiforme short shoots, leaves, and leaf 

length found within the productivity quadrats were recorded. 

Epiphytic material, including inorganic carbonates, adhering 

to T. testudinum leaves was removed by gentle scraping with 

a razor blade. Epiphytes were placed into preweighed 20-ml 

glass scintillation vials and stored at -20?C. Seagrass leaf 

material within each productivity quadrat was pooled by species, dried at 70?C, and ground to a fine powder. Carbon and 

nitrogen contents were determined with a CHN analyzer (Fisons NA1500). Phosphorus content was determined by a 

dry-oxidation, acid hydrolysis extraction followed by colorimetric analysis of phosphate concentration (Fourqurean et 

al. 1992). Elemental content and ratios were calculated on a 

dry weight and mole: mole basis, respectively. 

Epiphytes were freeze-dried to obtain dry weight, and total epiphyte load (g dry weight of epiphytes g-l dry weight 

of seagrass leaves) was determined. Twenty milliliters of 

90% acetone was added to each vial. Vials were shaken and 

stored at -20?C for a minimum of 72 h. Chl a content of 

the acetone extracts was measured fluorometrically (Strickland and Parsons 1972) on a Gilford Fluoro IV spectrofluorometer (excitation = 435 nm, emission = 667 nm). Epiphyte autotrophic content (/,g Chl a mg-' epiphyte) was 

used to estimate the relative contribution of algal epiphytism 

(Frankovich and Fourqurean 1997). 

Abundance of macrophytes (seagrasses and macroalgae) 

was assessed by the Braun-Blanquet procedure (Fourqurean 

et al. 2001). This technique results in a score of relative 

cover, in which cover is defined as the fraction of the bottom 

that is obscured by specific benthic taxa when viewed by a 

diver from directly above. Score values were as follows: 0, 

absent; 1, <5% cover; 2, 5-25% cover; 3, 25-50% cover; 

4, 50-75% cover; 5, 75-100% cover. 

Two sediment cores (1.15 cm diameter, 2.61 cm depth) 

were taken from each treatment plot. One core was used to 

estimate sediment microalgal abundance via determination 

of Chl a content of the sediment (mg Chl a m-2). Sediment 

samples were transferred into 20-ml glass scintillation vials 

and placed on ice in the dark. In the lab, 10 ml of 100% 

acetone was added to the wet sample to extract Chl a, and 

further analysis followed the method used for epiphyte Chl 

a content. The second core was used to analyze sediment 

porosity, bulk density, organic content, and elemental content (C, N, P). Sediment was transferred into preweighed 20- 

The sample was dried at 70?C for 48 h to obtain a dry 

weight. Dry samples were ground with a ceramic mortar and 

pestle. Sediment total nutrients were analyzed by the same 

methods as seagrass nutrients. Sediments were ashed at 

500?C for 5 h, and percent organic content was calculated 

as loss on ignition. 

T. testudinum rhizomes for nutrient analysis (C:N:P) 

were randomly collected from each quadrat, rinsed to remove carbonate sediments, dried at 70?C, ground to a fine 

powder, and analyzed in the method described above. Nonepiphytic macroalgal abundance was calculated for each 

treatment plot with a modification of the Braun-Blanquet 

quadrat method (Fourqurean et al. 2001). 

Retention efficiency calculations-Changes in community 

structure often occur on timescales greater than this experiment. In order to gain insight into the fate of added nutrients 

and the relative long-term importance of N and P additions, 

we estimated the retention efficiency of nitrogen and phosphorus in both nearshore and offshore seagrass systems. Absolute quantities of nitrogen and phosphorus were calculated 

for compartments within a 0.25-m3 (25 X 100 X 100 cm) 

seagrass habitat containing 200 liters of water column and 

50 liters of sediment. The following compartments were included: water column, T. testudinum leaves, T. testudinum 

rhizomes, S. filiforme leaves, nonepiphytic macroalgae, T. 

testudinum epiphytes, and sediment. Water quality data were 

obtained from the Southeast Environmental Research Center 

Water Quality Monitoring Network at Florida International 

University. Absolute quantities (g) of nitrogen and phosphorus in each component were calculated by multiplying nutrient content (percent dry weight) and total mass (g m-2). 

Estimates for macroalgal biomass (113 g dry weight m-2; 

Davis and Fourqurean 2001) and epiphyte nutrient content 

(N = 1.48% of ash free dry weight (AFDW), P = 0.22% of 

AFDW; Lin et al. 1996) were obtained from the literature. 

T. testudinum belowground biomass was estimated as 85% 

of total T. testudinum mass. The remaining data were derived 

directly from this experiment. Mass balances were calculated 

for control and +N+P treatments at both nearshore and offshore sites. Net system retention ([total system nutrient (g), 

+N+P] - [total system nutrient (g), control]) and retention 

efficiency ([net system retention (g)/mass applied (g)] X 

100%) were calculated. 

Results 

Nearshore and offshore waters exhibited similar mean water temperature and salinity (Table 1). There was an inverse 

relationship between depth and light attenuation: the deeper 

offshore sites had higher water clarity, as evidenced by lower 

light attenuation and lower turbidity, compared with nearshore sites. Despite the difference in water clarity, the 

amount of light reaching the benthos (% lo) was not very 

different between nearshore and offshore locations: between 

14.2% and 27.8% of the incoming solar radiation reached 

the seagrass canopy. Sediments at nearshore sites had higher 

porosity, lower bulk density, and higher organic content 

compared with offshore sites, which consisted of coarser 

ml glass scintillation vials, and wet weight was calculated. 

2085 

sand and a low contribution of organic material. Nearshore 
Ferdie and Fourqurean 

Table 1. Summary of site descriptions and environmental parameters. Temperature and salinity are annual means (n = 10-18). The 

diffuse attenuation coefficient (kd) and the amount of light reaching the benthos (% I,) are means of quarterly measurements from 1995 to 

2002 (n = 18-27). Turbidity was measured in Nephelometric Turbidity Units (NTU). Sediment characteristics and abundance values are 

site means (n = 24) from the beginning of the experiment. Differences in means between onshore and offshore sites were evaluated by ttests. Parameters with different means (p - 0.05) are bold. 

Nearshore Offshore t t-test 

I-1 1-2 I-3 O-1 0-2 0-3 p value 

Water 

Depth (m) 5 5 4 8 8 6 0.023 

Salinity 35.9 36.0 36.1 36.2 36.2 36.1 0.067 

Temperature (?C) 24.6 26.2 26.5 26.7 26.6 26.9 0.180 

Turbidity (NTU) 0.64 0.39 0.59 0.30 0.26 0.25 0.026 

Light attenuation, kd (m-1) 0.32 0.39 0.33 0.23 0.16 0.29 0.051 

Io (%) 20.2 14.2 26.7 15.9 27.8 17.6 0.990 

Sediment 

Porosity (g cm-3) 0.71 0.69 0.77 0.54 0.52 0.60 0.007 

Bulk density (g cm-3) 0.77 0.79 0.93 1.20 1.21 1.23 0.002 

Organic content (%) 4.52 3.78 3.47 2.25 2.07 1.91 0.005 

Macrophyte abundance 

Thalassia 3.1 4.0 3.9 3.9 3.7 3.6 0.834 

Syringodium 0.0 0.1 0.3 0.6 1.1 2.5 0.092 

Nonepiphytic macroalgae 1.5 1.0 1.0 0.1 0.8 1.4 0.386 

seagrass beds were dominated by T. testudinum interspersed 

with abundant mounds of fine mud deposited by infauna. 

Offshore seagrass beds were more homogeneous, and S. filiforme was more abundant in offshore compared with nearshore sites. T. testudinum rhizomes were primarily located 

in the top 10 cm of sediment at nearshore sites, whereas 

offshore rhizomes were found at greater depth (-5-20 cm). 

Nonepiphytic macroalgal composition consisted primarily of 

calcareous green algae species (Penicillus spp., Halimeda 

spp., Udotea spp., Rhipocephalus spp.). Also present in 

sparse amounts were green algae (e.g., Avrainvillea spp., 

Codium spp., Dasycladus spp., Batophora spp., Caulerpa 

spp.), red algae (e.g., Laurencia spp., Gracilaria spp.), and 

brown algae (e.g., Dictyota spp.). 

Seagrass morphology, standing crop, and growth responses Sediment fertilization increased sediment nutrient content and increased plant nutrient content, providing evidence 

that fertilization increased availability of both nitrogen and 

phosphorus. Plant nutrient enrichment resulted in significant 

changes in T. testudinum leaf nutrient content (Fig. 2) and 

elemental ratios (Fig. 3). Nitrogen addition led to rapid uptake of nitrogen by seagrass at both nearshore and offshore 

sites, as evidenced by increases in leaf N content and decreases in C:N. The response to P addition was delayed 

compared with N addition. Whereas the effects of N addition 

were evident at both nearshore and offshore sites in September 2001 (4 months of fertilization), elevated leaf P content 

was not observed at nearshore sites until March 2002 (10 

months) and at offshore sites until July 2002 (14 months). 

The nutrient contents of S. filiforme leaves and T. testudinum 

rhizomes were significantly affected by nutrient addition 

(Fig. 4). Nitrogen addition decreased S. filiforme leaf and T. 

testudinum rhizome C: N. Phosphorus addition decreased S. 

filiforme leaf C: P. Significant changes in rhizome P content 

and C: P values with P addition were observed at nearshore, 

but not offshore, sites. 

Nutrient addition significantly affected T. testudinum 

length, standing crop, and growth rates (Fig. 5). Leaf length, 

standing crop, and areal productivity increased with N addition at offshore sites, but not at nearshore sites. There were 

no significant effects of P addition on T. testudinum productivity. Nitrogen addition significantly increased S. filiforme 

length and standing crop at offshore, but not nearshore, sites 

(Fig. 6). There were no significant effects of nutrient additions on T. testudinum leaf emergence rates. 

Algal responses to nutrient enrichment occurred primarily 

at nearshore sites (Fig. 7). Nonepiphytic macroalgal abundance increased with N addition at nearshore sites only (significant Location X N interaction). Both N and P additions 

affected epiphyte loads, but in a complex manner (significant 

main effects of N and P additions on epiphyte load). Nearshore, P addition increased epiphyte loads, whereas offshore, 

N additions decreased loads on the seagrass blades. Additions of both nitrogen and phosphorus significantly increased 

the epiphyte Chl a content at inshore sites, but at offshore 

sites, only N addition increased the autotrophic index. Sediment microalgae abundance increased only with +N+P enrichment at nearshore sites. 

Retention efficiency of nitrogen and phosphorus-The relative allocation of nitrogen and phosphorus to various seagrass system compartments was similar between nearshore 

and offshore sites. However, the net retention of added nutrients varied considerably on the basis of nutrient and location (Table 2). The majority of nitrogen and phosphorus 

was located in the sediment, and the water column contribution was negligible (<0.1%). Nutrient enrichment nearly 

doubled both nearshore and offshore total nitrogen in the 

system, and greatly elevated total nearshore phosphorus and 

2086 
Fertilization of seagrass communities 

0.2 - 0.15 - 

^ T L E--- Nearshore 

E * | '====1 X Offshore 

q.a 2 0.10- 

0 . 

I IT T TI ??-TI 

= 0.05- 

0.0 0.00 

C +N +P +N+P C +N +P +N+P 

g 0.20 

2.5 

20 o 0.15- 2.0' 

....-~~~~~~~ .S 0.10- 

1.0 

C +N +P +N+P C +N +P +N+P 

Fig. 2. Phosphorus and nitrogen content of sediments and leaves of Thalassia testudinum at 

nearshore and offshore sites following 14 months of fertilization, expressed as percentage of dry 

weight. Values are treatment means (n = 18), and error bars are ? 1 SE. 

offshore phosphorus. Net system retention for both nitrogen Discussion 

and phosphorus were higher at nearshore sites compared 

with offshore sites. Retention efficiency was large for phos- This experiment demonstrated that nearshore benthic 

phorus (nearshore = 82%, offshore = 49%) and relatively communities in south Florida are indeed nutrient limited, but 

small for nitrogen (nearshore = 9%, offshore = 4%). the nature of that limitation differs for nearshore and off35 - 35 Nearshore Offshore 

30- 30- 

25 - 25 

| 20 - +N 20- 

-f- +N+P 

15 . . . 1 5 

May 01 Sep 01 Mar 02 July 02 May 01 Sep 01 Mar 02 July 02 

Nearshore Offshore 

1600 1600 - 

1200 1200 - 

800 800- 

400 . . 400 

May 01 Sep 01 Mar 02 July 02 May 01 Sep 01 Mar 02 July 02 

Fig. 3. Thalassia testudinum leaf nutrient ratios during the course of the experiments. Values 

are treatment means (n = 18), and error bars are 1 SE. 

2087 
Ferdie and Fourqurean 

C +N +P +N+P 

:. 1500 

U 

0 

*I 1000 

500 

3500 

U Co 

E 

o 

'= 2000 

t_ 

500 

I 

IL 

I 

.I 

L ; 

C +N +P +N+P 

C +N +P +N+P C +N +P +N+P 

Fig. 4. Thalassia testudinum rhizome and Syringodium filiforme leaf nutrient content responses 

at nearshore and offshore sites following 14 months of fertilization, expressed as percentage of dry 

weight. Values are treatment means (n = 18), and error bars are + 1 SE. Syringodium filiforme was 

not present in any +N treatments at nearshore sites. 

shore sites and for seagrass and algae (Table 3). The original 

hypothesis that seagrass communities are P-limited nearshore and N-limited offshore was partially supported by the 

responses of primary producers to nutrient enrichment. 

There was an increase in T. testudinunz leaf length, standing 

crop, and growth rates (Fig. 5) in response to N, but not P, 

addition at offshore sites. Offshore S. filiifrme leaf length 

and standing crop also increased with N addition. This implies that seagrass in offshore habitats in the upper Florida 

Keys are N-limited. Nutrient addition at nearshore sites had 

no significant effect on T. testudinum or S. filiforme length 

or standing crop. T. testudinum areal productivity at nearshore sites increased with +N and +N+P treatments, suggesting that nearshore T. testudinum might be nutrient limited, but this limitation is not as severe as offshore seagrass. 

Contrary to our a priori predictions based on stoichiometric 

evidence, there was no clear increase in biomass or primary 

productivity of seagrasses at nearshore sites in response to 

P addition. 

Significant increases in the relative abundance of nonseagrass primary producers were found almost exclusively at 

nearshore sites (Fig. 7) and encountered with all nutrient 

treatments (+N, +P, +N+P). Macroalgal abundance, total 

epiphyte load, epiphyte autotrophic content, and sediment 

microalgae abundance increased with nutrient addition at 

nearshore sites. A decrease in total epiphyte loads at offshore 

sites with +N and +N+P addition might have been caused 

by higher leaf production and leaf mass associated with offshore N addition. The only significant effect of nutrients on 

an offshore algal response variable was an increase in epiphyte Chl a content with N addition (+N, +N+P), although 

the increase was not as great in magnitude as the nearshore 

response. This suggests that the autotrophic component of 

the offshore epiphyte complex might be N-limited, as was 

observed for the offshore seagrass. 

The strong epiphyte responses at nearshore sites might be 

a function of benthic microalgal mats. Qualitative observations by divers of microalgal blooms were identified exclusively in nutrient treatments (+N, +P, +N +P) at nearshore, 

but not offshore, sites. The absence of benthic algae increases at offshore sites might be a result of higher water energy 

and strong water mixing at offshore sites, which might have 

physically inhibited the development of benthic microalgal 

mats, or of observation times that do not coincide with mat 

formation, or of microalgal mats that are not nutrient limited 

at offshore sites. The dynamics of benthic microalgae in response to nutrient enrichment deserve more attention in future research. 

The competitive outcome following changes in nutrient 

availability plays a critical role in determining the community response to eutrophication. Although the time frame of 

this experiment was not long enough to observe community 

structure shifts, changes in the relative abundance of primary 

producers allowed us to predict the future trajectory of community composition. Increases in S. filiforme, macroalgae, 

and epiphyte abundance observed in this study might lead 

to direct competition with T. testudinum for resources. Mean 

leaf length for S. filiforme in offshore +N+P treatments (198 

+ 48 mm) were higher than T. testudinum (176 + 39 mm), 

suggesting that shading effects on T. testudinum by S. filiforme can occur with fertilization. These shading effects 

might be exacerbated by a higher T. testudinum minimum 

light requirement than S. filiforme (Wiginton and McMillan 

1979). Macroalgal species, especially rhizophytic calcareous 

35 

25 

15 

100 

4 

E 0 

-N 

L. 60 

20 

l 11 

2088 
Fertilization of seagrass communities 

Nearshore 180 - 

160 - 

140 - 

120 - 

100 - 

80 

May01 Sep01 Mar 02 July 02 

Nearshore 

Sep01 Mar02 July02 

Nearshore 

* C 

---- +N 

- +N+P 

*- +P 

180 

160 

140 

120 

100 

80 

60 

40 

4- 

3- 

Offshore 

May01 Sep01 Mar 02 July 02 

Sep01 Mar 02 July 02 

Offshore I 

1 

Sep01 Mar 02 July 02 Sep01 Mar02 July02 

Fig. 5. Morphology and growth measurements of Thalassia testudinum over the course of the 

experiments at nearshore and offshore sites. Values are treatment means (n = 18), and error bars 

are 1 SE. 

225- 

E 

150' 

.iz 75 

C2 75- 

1 - Nearshore 

r 'l Offshore 

I 

c +N +P +N+P 

E 50 

0 

._ 

m 25- 

r: 

E0 

OC 

I 

I 

I 

+N+P 

Fig. 6. Syringodium filiforme mean leaf length and standing crop at nearshore and offshore sites 

following 14 months of fertilization. Values are treatment means (n = 18), and error bars are ?_1 

SE. 

180 

E 160 

140 

, 120 

; 100 

80 

180 

' 160 

a 140 

0 120 

a 100 

I 80 

60 

40 

4 

3 

2 

E 

b-D 

c) 

-0 

L 

1. 

< 

1 

w 

I .I 

-_ M_ ------- t MM 

2089 

?.: 

1 

1t 

i, 
Ferdie and Fourqurean 

Nearshore 

1.5- = Offshore 

s 1.0 

0 0.5 

0.0 

C +N +P +N+P 

= 220- 

o | 2 

* 

. 160- 

100 

C +N +P +N+P 

0.6- 

0.4 

5 tT,l, ;q 

,; ?. m ,i | K 

U.z 

60 

E 

. 45 

E 

30 

Fig. 7. Epiphyte load and autotrophic content and nonepiphytic macroalgal and sediment microalgal responses at nearshore and offshore sites following 14 months of fertilization. Values are 

treatment means (n = 18), and error bars are ? 1 SE. 

greens, are conspicuous in south Florida seagrass communities and might compete with seagrasses for light, space, 

and nutrients (Davis and Fourqurean 2001). Seagrasses are 

especially prone to the negative shading effects of epiphytes 

and benthic algal blooms (e.g., Twilley et al. 1985). Nutrient 

enrichment in this experiment resulted in an increase in seagrass biomass at offshore sites and an increase in algal biomass at nearshore sites. This demonstrates that both regions 

are nutrient limited but that taxon-specific responses to nutrient enrichment are different. Continuous nutrient enrichment could lead to a shift from T. testudinum to S. filiforme 

dominance at offshore sites and to algae dominance at nearshore sites. 

The time course of seagrass community responses to 

changes in nutrient availability has been shown to occur on 

the scale of years and decades. In Florida Bay, a monoculture T. testudinum bed was replaced by H. wrightii following 

8 yr of fertilization (Fourqurean et al. 1995). Changes have 

also been shown to occur following the cessation of nutrient 

addition. In the Mediterranean, a Posidonia oceanica meadow displayed persistent seagrass declines 3 yr following the 

closure of a fish farm (Delgado et al. 1999). These long-term 

community changes suggest that nutrients were retained and 

recycled in the system. Benthic communities in this experiment differed dramatically in their retention of nitrogen and 

phosphorus (Table 2). Although total system nitrogen douTable 2. Absolute quantities (g) and retention efficiency (%) of nitrogen and phosphorus for compartments within 0.25 ml of seagrass 

habitat containing 200 liters of water column and 50 liters of sediment. Measurements are listed for control (C) and nutrient (+N+P) 

treatments at nearshore and offshore sites. 

Nitrogen Phosphorus 

Compo t Nearshore Offshore Nearshore Offshore 

Component 

[g (0.25 m-3)-'I C +N+P C +N+P C +N+P C +N+P 

Sediment 43.5 67.1 21.4 24.5 3.4 44.3 10.2 33.7 

Thalassia aboveground 1.7 2.2 1.2 2.6 0.1 0.1 0.1 0.2 

Thalassia belowground 3.4 7.8 2.4 10.6 0.2 0.4 0.4 1.0 

Syringodium leaves 0.1 0.4 0.1 0.9 0.003 0.03 0.01 0.05 

Macroalgae 0.3 0.3 0.3 0.3 0.04 0.04 0.04 0.04 

Epiphytes 0.4 0.6 0.6 0.7 0.07 0.1 0.1 0.1 

Water column 0.04 0.04 0.04 0.04 0.001 0.001 0.001 0.001 

Total system (g) 49.4 78.5 26.1 39.7 3.8 45.1 10.8 35.2 

Net retention (g) 29.1 13.6 41.2 24.4 

Mass applied (g) 323 323 50 50 

Retention efficiency (%) 9.0 4.2 82.5 48.7 

C +N +P +N+P 

iC + C +N +P +N+P 

l 

2090 
Fertilization of seagrass communities 

Table 3. A summary of statistically significant (ANOVA main effects, p 

- 0.05) responses after 14 months of fertilization. A plus (+) 

indicates that the variable was greater than the controls, a minus (-) indicates a decrease compared with controls. ND indicates there was 

no comparison possible, because Syringodium filiforme was absent from all +N treatments at the inshore locations. 

Nearshore Offshore 

Response variable +N +P +N+P +N +P +N+P 

Thalassia testudinum 

Areal productivity 

Specific productivity 

Productivity per short shoot 

Standing crop 

Leaf length 

Syringodium filiforme 

Standing crop 

Short shoot density 

Leaf length 

Macroalgae 

Abundance 

Epiphytes 

Load 

Chl a load 

Autotrophic index 

Sediment microalgae 

Abundance 

Nutrient content of seagrasses 

Thalassia 

Leaf N content 

Leaf P content 

Leaf C N 

Leaf C P 

Leaf N:P 

Rhizome N content 

Rhizome P content 

Rhizome C N 

Rhizome C: P 

Rhizome N: P 

Syringodium 

Leaf N content 

Leaf P content 

Leaf C: N 

Leaf C: P 

Leaf N:P 

+ 

+ + 

+ 

? 

+ 

ND 

ND 

ND 

+ 

+ 

+ 

+ 

+- 

+ + 

+ 

+ 

+ 

? - 

+ + 

+- + 4- 

+ 

+ 

+ 

+ + + 

+ 

+ 

+ 

+ 

+ 

+ 

+ 

ND 

ND 

ND 

ND 

ND 

+ 

+ 

+ 

+ 

+ 

+ + 

+ + 

+ 

+ 

+ + 

+ 

+ 

+ 

+ 

+ + 

+ + 

+ 

+ 

bled with N addition, <10% of the added nitrogen was retained. In contrast, these sites were extremely efficient at P 

retention: 82% and 49% of added phosphorus was retained 

at nearshore and offshore sites, respectively. These differences suggests that long-term P enrichment, unlike N enrichment, has the potential to be an important driver of longterm community changes because most of the phosphorus 

was retained within the system, whereas much of the nitrogen was lost from the system. Nutrients can be lost from a 

system via several pathways, including mineralization processes, sedimentation, diffusion from the sediment, physical 

removal, and herbivory. The sediment served as a large sink 

for phosphorus in this study. The high loss rates of nitrogen 

was likely a function of microbial transformations (e.g., denitrification). Because of the high affinity of carbonate sediments for phosphate, it is also likely that inorganic nitrogen 

is more mobile and therefore more easily lost from the system. 

Seagrass leaf nutrient content increased at all sites with 

the addition of nutrients, but the magnitude of these responses varied by time and location. Increases in T. testudinum 

leaf N content were apparent quickly (4 months of fertilization), whereas significant increases in P content were not 

observed at nearshore sites until 10 months and at offshore 

sites until 14 months (Fig. 3). The overall delayed response 

of T. testudinum leaf P content with P addition might have 

been caused by sorption of added phosphorus on carbonate 

sediments (Short et al. 1990). However, this geochemical 

process does not explain the difference between nearshore 

and offshore T. testudinum P content responses to +P ad2091 
Ferdie and Fourqurean 

dition. Sediment grain size has been shown to possess an 

inverse relationship to sorption potential: smaller grain sizes 

provide more surface area for P adsorption, resulting in less 

phosphorus available for plant uptake (Erftemeijer 1994). On 

the basis of this phenomenon, we could predict that nearshore sites, with smaller grain size, would display delayed 

P uptake by seagrass compared with offshore sites. The opposite pattern was observed. Dissolution and precipitation of 

carbonates are also influenced by organic matter (Morse et 

al. 1985) and sediment pH (Jensen et al. 1998), where 

CaCO3 dissolution is related to higher organic content. Nearshore sediments have relatively higher organic content (Table 1), so this factor might affect P availability. It is also 

possible that the greater depth of the root zone at offshore 

sites might account for the delay in seagrass P uptake. An 

alternate explanation is that P uptake by T. testudinum did 

not occur at offshore sites because phosphorus was not limiting. The increase of rhizome P content with +P at nearshore, but not offshore, sites is further evidence that phosphorus did not limit seagrass growth or metabolic processes 

at offshore sites (Fig. 4). 

The addition of nitrogen not only increased T. testudinum 

N content, but it also affected the metabolism and uptake of 

phosphorus. A significant decrease in leaf P content with N 

addition was observed at both nearshore and offshore sites 

(Figs. 2, 3). A probable explanation is that the addition of 

nitrogen increased N assimilation and led to higher P demand, a phenomena observed with nutrient enrichment in an 

Australian seagrass bed (Udy and Dennison 1997). This net 

decrease was not seen with +N+P, presumably because the 

increased P demand was met by fertilization. The addition 

of phosphorus alone did not have a significant negative effect on N content, emphasizing the difference in metabolic 

characteristics of specific nutrients. 

Growth and biomass responses in this experiment did not 

consistently follow the nutrient content responses. Although 

N addition increased leaf N content at all sites, increases in 

leaf length and standing crop were found only at offshore 

sites. The addition of phosphorus alone to nearshore and 

offshore sites increased leaf P concentrations but did not 

affect length, standing crop, or growth rates. Increases in T. 

testudinum leaf nutrient content in the absence of a positive 

standing crop or growth response implies that nutrient availability in the study area was either insufficient to satisfy all 

plant metabolic demands for nitrogen, phosphorus, or both, 

or that T. testudinum is capable of storing excess nutrients 

when demand is less than supply, also known as luxury consumption. Luxury consumption of nutrients by algae is common (e.g., Campbell 2001) and has also been identified in 

seagrass (e.g., Murray et al. 1992; Van Lent et al. 1995). 

Nutrient storage differs between T. testudinum photosynthetic (leaves) and structural (rhizomes) tissues; the photosynthetic short shoots contain the largest amount of nitrogen 

and phosphorus, whereas rhizomes serve as important carbohydrate storage organs. The only instance in this study in 

which the addition of a solitary nutrient (N or P) had no 

effect on plant nutrient content for that particular nutrient 

was for rhizome C: P and P content (Fig. 4) at offshore sites. 

The absence of a rhizome P increase might be a function of 

accessibility, in which the added phosphorus did not migrate 

downward to the relatively deep rhizome-root complex because of sorption activity, relatively lower mobility, or both 

compared with nitrogen. It is also possible that the added 

phosphorus was not integrated into offshore rhizome tissue 

because the element is in excess at offshore sites and not 

required, which is likely because offshore P availability is 

relatively high and offshore growth is strongly N-limited. 

Ecological applications of this study-Phosphorus limitation of coastal primary production is frequently associated 

with tropical marine carbonate systems in which the strong 

sorption affinity of phosphorus to calcium carbonate mineral 

surfaces reduces the amount of phosphorus available for 

plant uptake (Morse et al. 1985). Biological availability of 

phosphorus is further regulated by geochemical processes, 

such as sediment grain size (Erftemeijer 1994), sorption-site 

saturation (McGlathery et al. 1994), and carbonate dissolution dynamics (e.g., Jensen et al. 1998; Burdige and Zimmerman 2002). There is building evidence that seagrass 

communities found in carbonate-rich systems can be limited 

by nitrogen rather than phosphorus. A review of in situ seagrass fertilization experiments that included separate N and 

P enrichment found only one out of seven studies which 

clearly identified P limitation of seagrass growth in a carbonate system (Table 4). In this frequently cited investigation, Short et al. (1990) found significant effects of P addition on S. filiforme growth only when porewater P 

concentrations were increased to 2,000 times ambient levels, 

a concentration that might be excessive in real-life scenarios. 

Other fertilization experiments that used only +N+P combined addition have inferred P limitation with changes in 

leaf nutrient content, biomass measurements, or both (Agawin et al. 1996; Powell et al. 1989), but at this time, adequate 

experimental data is lacking to justify a broad assumption 

of P limitation in carbonate systems. In temperate systems, 

three out of six fertilization studies identified seagrass 

growth with P addition (Harlin and Thorne-Miller 1981; 

Perez et al. 1991; Murray et al. 1992), suggesting that P 

limitation is more common on a global scale and that parameters such as locale (tropical vs. temperate) and sediment 

composition (carbonate contribution) are not effective predictors of seagrass nutrient limitation. This experiment clearly demonstrated N limitation of T. testudinum and S. filiforme in the offshore waters of the upper Florida Keys, despite 

predictions of P limitation in carbonate systems. 

This study partially supports our original hypotheses of 

nutrient limitation on the basis of patterns of nutrient availability: nearshore algae were affected by nitrogen and phosphorus, and offshore seagrasses were affected by nitrogen. 

Predictions of nearshore P limitation were not strongly supported by our experimental results. It is possible that nearshore habitats are P-limited, but the signal was not observed 

because of factors such as the relatively short experimental 

time period, high nutrient conservation, and recycling of T. 

testudinum as an adaptation to low nutrient environments. 

These problems are associated with P-loading, sediment 

sorption, or the indirect effects of microalgal mats, which 

can cause direct shading of seagrass photosynthetic tissue or 

affect sediment processes such as oxygen demand. Predicting the response of a system to eutrophication is confounded 

2092 
Fertilization of seagrass communities 

Table 4. Responses of seagrass to in situ nutrient enrichment experiments involving separate nitrogen (N) and phosphorus (P) addition. 

Entries are grouped by climate (temperate vs. tropical/subtropical) and by sediment regime (carbonate vs. siliciclastic). 

Response 

Location Species Tissue Growth Source 

Tropical/subtropical carbonate 

Indonesia (coral islands) Thalassia hemprichii +N None Erftemeijer et al. (1994) 

Bahamas Syringodium filiforme +N+P +P Short et al. (1990) 

NE Australia Halodule uninervis +N +N Udy et al. (1999) 

NE Australia Syringodium isoetifolium +N +N Udy et al. (1999) 

Florida Keys Thalassia testudinum +N+P +N This investigation, offshore 

Florida Keys T. testudinum +N+P +N+P This investigation, nearshore 

Tropical/subtropical siliciclastic 

Indonesia (coastal site) T. hemprichii None None Erftemeijer et al. (1994) 

E Australia H. univervis +N +N Udy and Dennison (1997) 

E Australia Zostera capricorni +N+P +N+P Udy and Dennison (1997) 

E Australia Cymodocea serrulata +N None Udy and Dennison (1997) 

Temperate carbonate 

NE Spain Cymodocea nodosa +P +P Perez et al. (1991) 

Temperate siliciclastic 

SE Australia Heterozostera tasmanica +N+P +N Bulthuis et al. (1992) 

Italy C. nodosa None None Ceccherelli and Cinelli (1999) 

Rhode Island Zostera marina +N +N+P Harlin and Thorne-Miller (1981) 

Chesapeake Bay Z. marina +P +P Murray et al. (1992) 

by the fact that primary producers in coastal systems have 

species-specific nutrient requirements and can exhibit dissimilar forms of limitation. The limiting nutrient has been 

shown to vary among trophic levels such as plants and bacteria in coastal ecosystems (Sundareshwar et al. 2003), but 

this study clearly demonstrates that members within a trophic level might also respond differently to N and P enrichment. The response of seagrass communities in the upper 

Florida Keys to N and P enrichment varies appreciably between the nearshore and offshore environment, and the responses of all primary producers should be considered before categorizing a natural system with a specific nutrient 

limitation. 

References 

AGAWIN, N. S. R., C. M. DUARTE, AND M. D. FORTES. 1996. Nutrient limitation of Philippine seagrasses (Cape Bolinao, NW 

Philippines): in situ experimental evidence. Mar. Ecol. Prog. 

Ser. 138: 233-243. 

ATKINSON, M. J., AND S. V. SMITH. 1983. C:N:P ratios of benthic 

marine plants. Limnol. Oceanogr. 28: 568-574. 

BEDFORD, B. L., M. R. WALBRIDGE, AND A. ALDOUS. 1999. Patterns 

in nutrient availability and plant diversity of temperate north 

American wetlands. Ecology 80: 2151-2169. 

BOYER, J. N., AND R. D. JONES. 2002. View from the bridge: External and internal forces affecting the ambient water quality 

of the Florida Keys National Marine Sanctuary, p. 609-628. 

In J. W. Porter and K. G. Porter [eds.], The Everglades, Florida 

Bay, and Coral Reefs of the Florida Keys: An ecosystem 

sourcebook. CRC Press. 

BULTHUIS, D. A., D. M. AXELRAD, AND M. J. MICKELSON. 1992. 

Growth of the seagrass Heterozostera tasmanica limited by 

nitrogen in Port Phillip Bay, Australia. Mar. Ecol. Prog. Ser. 

89: 269-275. 

BURDIGE, D. J., AND R. C. ZIMMERMAN. 2002. Impact of seagrass 

density on carbonate dissolution in Bahamian sediments. Limnol. Oceanogr. 47: 1751-1763. 

CAMPBELL, S. 2001. Ammonium requirements of fast-growing 

ephemeral macroalgae in a nutrient-enriched marine embayment (Port Phillip Bay, Australia). Mar. Ecol. Prog. Ser. 209: 

99-107. 

CECCHERELLI, G., AND E CINELLI. 1999. A pilot study of nutrient 

enriched sediments in a Cymodocea nodosa bed invaded by 

the introduced alga Caulerpa taxifolia. Bot. Mar. 42: 409-417. 

DAVIS, B. D., AND J. W. FOURQUREAN. 2001. Competition between 

the tropical alga, Halimeda incrassata, and the seagrass, Thalassia testudinum. Aquat. Bot. 71: 217-232. 

DELGADO, O., J. RUIZ, M. PEREZ, J. ROMERO, AND E. BALLESTEROS. 

1999. Effects of fish farming on seagrass (Posidonia oceanica) 

in a Mediterranean bay: Seagrass decline after organic loading 

cessation. Oceanol. Acta 22: 109-117. 

DUARTE, C. M. 1990. Seagrass nutrient content. Mar. Ecol. Prog. 

Ser. 67: 201-201. 

. 1995. Submerged aquatic vegetation in relation to different 

nutrient regimes. Ophelia 41: 87-112. 

[EPA] U.S. ENVIRONMENTAL PROTECTION AGENCY. 1999. Water 

quality concerns in the Florida Keys: Sources, effects and solutions. EPA. 

ERFTEMEIJER, P. L. A. 1994. Differences in nutrient concentrations 

and resources between seagrass communities on carbonate and 

terrigenous sediments in South Sulawesi, Indonesia. Bull. Mar. 

Sci. 54: 403-419. 

, J. STAPEL, M. J. E. SMEKENS, AND W. M. E. DROSSAERT. 

1994. The limited effect of in situ phosphorus and nitrogen 

additions to seagrass beds on carbonate and terrigenous sediments in South Sulawesi, Indonesia. J. Exp. Mar. Biol. Ecol. 

182: 123-140. 

FENCHEL, T., AND T. H. BLACKBURN. 1979. Bacteria and mineral 

cycling. Academic. 

FOURQUREAN, J. W., AND J. C. ZIEMAN. 2002. Seagrass nutrient 

2093 
Ferdie and Fourqurean 

content of the seagrass Thalassia testudinum reveals regional 

patterns of relative availability of nitrogen and phosphorus in 

the Florida Keys USA. Biogeochemistry 61: 229-245. 

, AND G. V. N. POWELL. 1992. Relationships between porewater nutrients and seagrasses in a subtropical carbonate environment. Mar. Biol. 114: 57-65. 

, G. V. N. POWELL, W. J. KENWORTHY, AND J. C. ZIEMAN. 

1995. The effects of long-term manipulation of nutrient supply 

on competition between the seagrasses Thalassia testudinum 

and Halodule wrightii in Florida Bay. Oikos 72: 349-358. 

, A. WILLSIE, C. D. ROSE, AND L. M. RUTTEN. 2001. Spatial 

and temporal pattern in seagrass community composition and 

productivity in south Florida. Mar. Biol. 138: 341-354. 

, M. J. DURAKO, M. O. HALL, AND L. N. HEFTY. 2002. 

Seagrass distribution in south Florida: A multi-agency coordinated monitoring program, p. 497-522. In J. W. Porter and 

K. G. Porter [eds.], The Everglades, Florida Bay, and coral 

reefs of the Florida Keys. CRC Press. 

FRANKOVICH, T. A., AND J. W. FOURQUREAN. 1997. Seagrass epiphyte loads along a nutrient availability gradient, Florida Bay, 

USA. Mar. Ecol. Prog. Ser. 159: 37-50. 

HARLIN, M. M., AND B. THORNE-MILLER. 1981. Nutrient enrichment of seagrass beds in a Rhode Island coastal lagoon. Mar. 

Biol. 65: 221-229. 

HILLEBRAND, H., AND U. SOMMER. 1999. The nutrient stoichiometry of benthic microalga growth: Redfield proportions are optimal. Limnol. Oceanogr. 44: 440-446. 

HOWARTH, R. W. 1988. Nutrient limitation of net primary production in marine ecosystems. Ann. Rev. Ecol. Syst. 19: 89-110. 

JENSEN, H., K. MCGLATHERY, R. MARINO, AND R. HOWARTH. 1998. 

Forms and availability of sediment phosphorus in carbonate 

sand of Bermuda seagrass beds. Limnol. Oceanogr. 43: 799- 

810. 

JONES, R. D., AND J. N. BOYER. 2001. Annual report of the water 

quality monitoring project for the Florida Keys National Marine Sanctuary. Southeast Environmental Research Center. 

LIN, H. J., S. W. NIXON, D. I. TAYLOR, S. L. GRANGER, AND B. A. 

BUCKLEY. 1996. Response of epiphytes on eelgraass, Zostera 

marina L., to separate and combined nitrogen and phosphorus 

enrichment. Aquat. Bot. 52: 243-258. 

LYNGBY, J. E., S. MORTENSEN, AND N. AHRENSBERG. 1999. Bioassessment techniques for monitoring of eutrophication and nutrient limitation in coastal ecosystems. Mar. Pollut. Bull. 39: 

212-233. 

MCGLATHERY, K. J., R. MARINO, AND R. W. HOWARTH. 1994. Variable rates of phosphate uptake by shallow marine carbonate 

sediments-mechanisms and ecological significance. Biogeochemistry 25: 127-146. 

[MCSM] Monroe County Stormwater Management. 2001. Monroe 

county stormwater management master plan. V. 1. Data compilation and assessment report/objectives, standards and problem area ranking. MCSM. 

MORSE, J. W., AND OTHERS. 1985. Chemistry of calcium carbonaterich shallow water sediments in the Bahamas. Am. J. Sci. 285: 

147-185. 

MURRAY, L., W. C. DENNISON, AND W. M. KEMP. 1992. Nitrogen 

versus phosphorus limitation for growth of an estuarine population of eelgrass (Zostera marina L.). Aquat. Bot. 44: 83- 

100. 

PEREZ, M., J. ROMERO, C. M. DUARTE, AND K. SAND-JENSEN. 1991. 

Phosphorus limitation of Cymodocea nodosa growth. Mar. 

Biol. 109. 

POWELL, G. V. L., J. KENWORTHY, AND J. W. FOURQUREAN. 1989. 

Experimental evidence for nutrient limitation of seagrass 

growth in a tropical estuary with restricted circulation. Bull. 

Mar. Sci. 44: 324-340. 

REDFIELD, A. C. 1958. The biological control of chemical factors 

in the environment. Am. Sci. 46: 561-600. 

SHORT, E T. 1987. Effects of sediment nutrient on seagrasses: Literature review and mesocosm experiment. Aquat. Bot. 27: 41- 

57. 

,W. C. DENNISON, AND D. G. CAPONE. 1990. Phosphoruslimited growth of the tropical seagrass Syringodium filiforme 

in carbonate sediments. Mar. Ecol. Prog. Ser. 62: 169-174. 

STRICKLAND, J. D. H., AND T R. PARSONS. 1972. A practical handbook of seawater analysis. Bull. Fish. Res. Board Can. 44: 

179-199. 

SUNDARESHWAR, P. V., J. T. MORRIS, E. K. KOEPFLER, AND B. 

FORNWALT. 2003. Phosphorus limitation of coastal ecosystem 

processes. Science 299: 563-565. 

SZMANT, A. M., AND A. FORRESTER. 1996. Water column and sediment nitrogen and phosphorus distribution patters in the Florida Keys. Coral Reefs 15: 21-41. 

TERRADOS, J., N. S. R. AGAWIN, C. M. DUARTE, M. D. FORTES, L. 

KAMP-NIELSEN, AND J. BORUM. 1999. Nutrient limitation of 

the tropical seagrass Enhalus acoroides (L.) Royle in Cape 

Bolinao, NW Philippines. Aquat. Bot. 65: 123-139. 

TILMAN, D. 1982. Resource competition and community structure. 

Princeton Univ. Press. 

TWILLEY, R. R., M. W. KEMP, K. W. STAVER, J. C. STEVENSON, 

AND W. R. BOYNTON. 1985. Nutrient enrichment of estuarine 

submersed vascular plant communities. I. Algal growth and 

effects on production of plants and associated communities. 

Mar. Ecol. Prog. Ser. 23: 179-191. 

UDY, J. W., AND W. C. DENNISON. 1997. Growth and physiological 

responses of three seagrass species to elevated sediment nutrients in Moreton Bay, Australia. J. Exp. Mar. Biol. Ecol. 217: 

253-277. 

, C. D. WILLIAM, W. J. LEE HONG, AND L. J. MCKENZIE. 

1999. Responses of seagrass to nutrients in the Great Barrier 

Reef, Australia. Mar. Ecol. Prog. Ser. 185: 257-271. 

VALIELA, I., AND OTHERS. 1992. Couplings of watersheds and coastal waters-sources and consequences of nutrient enrichment in 

Waquoit Bay, Massachusetts. Estuaries 15: 443-457. 

VAN LENT, F, J. M. VERSCHUURE, AND M. L. J. VAN VEGHEL. 1995. 

Comparative study on populations of Zostera marina L. (eelgrass): In situ nitrogen enrichment and light manipulation. J. 

Exp. Mar. Biol. Ecol. 185: 55-76. 

WIGINTON, J. R., AND C. MCMILLAN. 1979. Chlorophyll composition under controlled light conditions as related to the distribution of seagrasses in Texas and the U.S. Virgin Islands. 

Aquat. Bot. 6: 171-184. 

WILLIAMS, S. L. 1990. Experimental studies of Caribbean seagrass 

bed development. Ecol. Monogr. 60: 449-469. 

Received: 30 May 2003 

Amended: 14 May 2004 

Accepted: 14 May 2004 

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