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«Anthropogenic nutrient enrichment of seagrass and coral reef communities in the Lower Florida Keys: discrimination of local versus regional nitrogen ...»

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Journal of Experimental Marine Biology and Ecology

308 (2004) 23 – 58

www.elsevier.com/locate/jembe

Anthropogenic nutrient enrichment of seagrass and

coral reef communities in the Lower Florida Keys:

discrimination of local versus regional

nitrogen sources

Brian E. Lapointe *, Peter J. Barile, William R. Matzie

Marine Nutrient Dynamics Program, Division of Marine Science, Harbor Branch Oceanographic Institution,

Inc., 5600 US 1 North, Ft. Pierce, FL 34946, USA Received 22 August 2003; received in revised form 16 January 2004; accepted 28 January 2004 Abstract Land-based nutrient pollution represents a significant human threat to coral reefs globally. We examined this phenomenon in shallow seagrass and coral reef communities between the Content Keys (southern Florida Bay) and Looe Key (south of Big Pine Key) in the Lower Florida Keys by quantifying the role of physical forcing (rainfall, wind, tides) and water management on mainland South Florida to nutrient enrichment and blooms of phytoplankton, macroalgae, and seagrass epiphytes. Initial studies (Phase I) in 1996 involved daily water quality sampling (prior to, during, and following physical forcing events) at three stations (AJ, an inshore area directly impacted by sewage discharges; PR, a nearshore patch reef located inshore of Hawk Channel; and LK, an offshore bank reef at Looe Key) to assess the spatial and temporal patterns in advection of land-based nutrients to the offshore reefs. Concentrations of dissolved inorganic nitrogen (DIN = NH+ + NOÀ + NOÀ), soluble reactive phosphorus (SRP), and chlorophyll a increased at PR and LK following a wind event ( f 15 knots, northeast) in mid-February. The highest DIN (mostly NH+) and SRP concentrations of the entire study occurred at the inshore AJ during an extreme low tide in March. Following the onset of the wet season in May, mean NH+ and chlorophyll a concentrations increased significantly to maximum seasonal values at PR and LK during summer; relatively low concentrations of NOÀ and a 3 low f-ratio (NOÀ/NH+ + NOÀ) at all stations during summer do not support the hypothesis that the seasonal phytoplankton blooms resulted from upwelling of NOÀ. A bloom of the seagrass epiphyte Cladosiphon occidentalis (phaeophyta) followed the onset of the rainy season and increased NH+ 4 concentrations at LK, resulting in very high epiphyte:blade ratios ( f 3:1) on Thalassia testudinum.

Biomass of macroalgae increased at all three stations from relatively low values ( 50 g dry wt mÀ 2) * Corresponding author. Tel.: +1-772-465-2400x276; fax: +1-772-468-0757.

E-mail address: lapointe@hboi.edu (B.E. Lapointe).

0022-0981/$ - see front matter D 2004 Elsevier B.V. All rights reserved.

doi:10.1016/j.jembe.2004.01.019 24 B.E. Lapointe et al. / J. Exp. Mar. Biol. Ecol. 308 (2004) 23–58 in winter and early spring to higher values ( f 100 – 300 g dry wt mÀ 2) typical of eutrophic seagrass meadows and coral reefs following the onset of the rainy season. The mean d15N value of Laurencia intricata (rhodophyta) during 1996 at AJ ( + 4.7x) was within the range reported for macroalgae growing on sewage nitrogen; lower values at the more offshore PR ( + 3.1x) and LK ( + 2.9x) were at the low end of the sewage range, indicating an offshore dilution of the sewage signal during the 1996 study. However, transient increases in d15N of Cladophora catanata (chlorophtyta) from ~ + 2% to + 5% at LK concurrent with elevated NH+ concentrations following rain and/or wind events in May and July suggest episodic advection of sewage nitrogen to the offshore LK station. The Phase II study involved sampling of macroalgae for d15N along a gradient from the Content Keys through Big Pine Key and offshore to LK in the summer wet season of 2000 and again in the drought of spring 2001.

During the July 2000 sampling, macroalgae in nearshore waters around Big Pine Key had elevated d15N values (~ + 4x) characteristic of sewage enrichment; lower values (~ + 2x) at LK were similar to values reported for macroalgae in upstream waters of western Florida Bay influenced by nitrogenrich Everglades runoff. That pattern contrasted with the drought sampling in March 2001, when d15N values of macroalgae were elevated ( + 6x) to levels characteristic of sewage enrichment over a broad spatial scale from the Content Keys to LK. These results suggest that regional-scale agricultural runoff from the mainland Everglades watersheds as well as local sewage discharges from the Florida Keys are both significant nitrogen sources supporting eutrophication and algal blooms in seagrass and coral reef communities in the Lower Florida Keys. Hydrological and physical forcing mechanisms, including rainfall, water management on the South Florida mainland, wind, and tides, regulate the relative importance and variability of these anthropogenic nitrogen inputs over gradients extending to the offshore waters of the Florida Reef Tract.

D 2004 Elsevier B.V. All rights reserved.

Keywords: Nitrogen; Phosphorus; Eutrophication; Coral; Seagrass; Phytoplankton; Macroalgae

1. Introduction Recognition of the critical interrelationships between water quality, the health of seagrass and coral reef communities, and economic well-being of the Florida Keys led to its designation as an ‘‘Area of Critical State Concern’’ by the Florida Legislature in





1974. Much of the concern centered around the potential impacts of excessive human development on coastal pollution and degradation of water quality. Three decades ago planners recognized that ‘‘the high quality of water in and around the Florida Keys is an essential element of the total system. One of the strongest attractions for residents and visitors to the area is the clear, blue waters of the Keys—a resource that rarely exists off the heavily populated, industrialized cities of the mainland’’ (State of Florida, 1974).

Water quality degradation was also a primary issue leading to designation of the Florida Keys National Marine Sanctuary (FKNMS) in 1990 that specifically included a multiagency (National Oceanic and Atmospheric Administration, NOAA; United States Environmental Protection Agency, USEPA; Florida Department of Environmental Protection, FDEP) Water Quality Protection Program (WQPP) for the FKNMS (NOAA, 1988;

USEPA, 1996). Of particular concern was the impact of local land-based sewage discharges, especially ecological damage from nutrient enrichment and eutrophication (Lapointe and Clark, 1992; Kruczynski and McManus, 2002). Currently, there are f 30,000 on-site sewage disposal systems (OSDSs; septic tanks, cesspits, and Class V B.E. Lapointe et al. / J. Exp. Mar. Biol. Ecol. 308 (2004) 23–58 25 injection wells cased to 28 m) in subdivisions scattered throughout the Florida Keys (Kruczynski and McManus, 2002). Most of these OSDSs are located adjacent to constructed canal systems that were designed to provide boating access to coastal waters that contain nutrient-sensitive seagrass and coral reef communities (NRC, 2000; Howarth et al., 2000). In addition to OSDSs, the City of Key Colony Beach (1.3 million l/day) and Key West (37 million l/day) have central sewage collection and treatment to secondary and tertiary levels, respectively, prior to injecting into Class V wells (Key Colony Beach) and Class 1 wells (cased to f 950 m, Key West).

A growing body of scientific evidence suggests an increasing impact of sewage pollution on degradation of water quality in the FKNMS. Because of high groundwater tables and transmissive limestone substrata, OSDSs in the Florida Keys rapidly contaminate groundwaters with high concentrations of dissolved inorganic nitrogen À À + (DIN = NH4 + NO3 + NO2 ) and to a lesser extent, soluble reactive phosphorus (SRP), which enter coastal waters via submarine groundwater discharge (SGD; Lapointe et al., 1990; Reich et al., 2002). Shinn et al. (1994) examined the fate and pathways of Class V injection well effluent using core drilled monitoring wells and found fecal contamination of groundwaters in three offshore wells in the Lower Florida Keys (Shinn et al., 1994).

Lapointe and Matzie (1996) used high-frequency monitoring of dissolved nutrients, salinity, temperature, and dissolved oxygen to track offshore advection of land-based + nutrient discharges of NH4 and SRP at the onset of the summer wet season in 1992; this + seasonal stormwater phenomenon, identified by decreased salinity and increased NH4 and SRP concentrations, initiated phytoplankton blooms and hypoxia over a broad spatial scale extending from sewage-impacted inshore waters on the west side of Big Pine Key to offshore waters at Looe Key. The problem of sewage pollution is not only one of eutrophication and loss of biotic resources, but also public health because of the known bacterial contamination of shallow groundwaters and contiguous surface waters by OSDSs (Paul et al., 1995a). Paul et al. (1995b), using viral tracers, found that wastewater transport from septic tanks through Key Largo limestone into adjacent surface waters ( f 20 m horizontal distance) occurred in as little as 11 h.

Excessive biomass of macroalgae is a common symptom of nutrient enrichment and eutrophication in seagrass and coral reef ecosystems (NRC, 2000; Howarth et al., 2000).

+ Because macroalgae can rapidly assimilate pulses of NH4 and SRP from the water column (D’Elia and DeBoer, 1978; Hanisak and Harlin, 1978), anthropogenic nutrient pollution can result in expansive blooms in oligotrophic tropical and subtropical waters (Banner, 1974; Johannes, 1975; Lapointe et al., 1994; Bell and Elmetri, 1995; Duarte, 1995;

Lapointe, 1997). Macroalgal blooms can physically overgrow seagrasses and adult corals, inhibit recruitment of juvenile corals, lead to hypoxia and/or anoxia, and result in greatly diminished fisheries and biological diversity (NRC, 2000; Howarth et al., 2000). Because of these detrimental effects, excessive biomass levels of macroalgae (above what would be considered ‘‘normal’’ for a particular species in a given environment) are considered Harmful Algal Blooms (HABs; ECOHAB, 1995). Over the past two decades, the Florida Reef Tract has experienced dramatic increases in cover of macroalgae with parallel losses of hard coral cover (Porter and Meier, 1992; Chiappone and Sullivan, 1997; Porter et al., 2002). At Looe Key reef, south of Big Pine Key in the Lower Florida Keys, this ‘‘phaseshift’’ away from hermatypic corals and towards dominance by macroalgae and algal turfs 26 B.E. Lapointe et al. / J. Exp. Mar. Biol. Ecol. 308 (2004) 23–58 has correlated with increasing annual mean concentrations of DIN and SRP despite the presence of high grazing by abundant schools of Scarid (parrotfishes) and Acanthurid (surgeonfishes) icthyofauna (Lapointe et al., 2002).

Seagrass and coral reef ecosystems impacted by nutrient pollution can require extensive recovery times (Smith et al., 1981; Duarte, 1995). Taxonomic shifts have been used as indicators of nutrient pollution on coral reefs (Littler, 1973; Johannes, 1975; Lapointe, 1997) but because the appearance of ‘‘indicator species’’ often signals an advanced stage of the problem, considerable environmental damage is likely to have already occurred. Measurement of stable nitrogen isotopes (15N/14N = d15N) in biota has been used widely to discriminate between natural and anthropogenic nitrogen sources (Heaton, 1986; Risk et al., 2001) and could provide an ‘‘early warning’’ tracer of anthropogenic nutrient enrichment such as from sewage or agricultural runoff. For reef corals, tissue is typically enriched in 15N by up to + 5x at sewage polluted, eutrophied sites relative to reference sites (Risk et al., 1993; Mendes et al., 1997;

Heikoop et al., 2000). Similar levels of enrichment in 15N have been reported for reef macroalgae experiencing sewage pollution. On coral reefs in the Negril Marine Park, Jamaica, macroalgae on shallow, sewage-impacted reefs had enriched d15N values ranging from + 4.0x to + 6.5x; macroalgae on deeper reefs less impacted by sewage had lower values of + 0.5x to + 2. 5x (Lapointe and Thacker, 2002; Table 1). On eutrophic coral reefs off southeast Florida, d15N values in Codium isthmocladum

–  –  –

increased from ~ + 5x to + 11x following heavy summer rainfall and increased discharges of sewage-contaminated groundwaters enriched in 15N into the Loxahatchee River and coastal waters (Lapointe, 1997; Table 1). Costanzo et al. (2001) recently reported that d15N values of macroalgae were enriched + 3x in areas of Moreton Bay, Brisbane, Australia, that were chronically impacted by sewage nitrogen. In comparison, 21 samples of tropical macroalgae had a mean d15N of + 0.5 F 1.0x in relatively unpolluted coastal waters of southwestern Puerto Rico, a value close to the atmospheric signature of 0x and indicative of nitrogen fixation as the source of nitrogen supporting growth (France et al., 1998; Table 1). We hypothesized that if wastewater DIN was impacting seagrass and coral reef communities in coastal waters of the Lower Florida Keys, then macroalgae inhabiting these habitats should have d15N values + 3x.

Other regional-scale sources of nitrogen with d15N signatures different from sewage could also simultaneously contribute to macroalgal HABs and water quality degradation in the FKNMS. Offshore upwelling of cold subsurface water has been hypothesized to be a À significant source of NO3 and SRP to coastal waters of the Florida Keys (Lapointe and Smith, 1987; Leichter et al., 1996; Szmant and Forrester, 1996; Leichter et al., 2003).

However, these deep, offshore cold water intrusions occur primarily in summer months as a result of wind forcing and are highly episodic; when they do occur, they have only À minor, if any, effects on NO3 concentrations in 30 m water depths in the FKNMS (Lapointe and Smith, 1987; Leichter et al., 1996, 2003). However, previous studies have shown significant long-term gradients in DIN and SRP concentrations from inshore to offshore waters of the FKNMS as a result of land-based nutrient inputs from the Florida Keys and mainland South Florida (Lapointe and Clark, 1992; Lapointe and Matzie, 1996;



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