Opporturzities atid Cl~allerlges for Protecti~lg, Restoring and Enirar~cirlg 

Coastcrl ifabitats in the Bay ofF~c~ldji 

NUTRIENT OVER-ENRICHMENT OF SOUTH FLORIDA'S CORAL REEFS: 

HOW SCIENCE AND MANAGEMENT FAILED TO PROTECT A 

NATIONAL TREASURE 

B.E. Lapointe 

Marine Nutrient Dynamics, Division of Marine Sciences, I-Iarbor Branch Oceanographic 

Institution, Inc., 5600 U.S. 1 North, Ft. Pierce, FL 34946, USA. lapointe@hboi.edu 

Introduction 

The Florida Keys are the most popular SCUBA diving and snorkeling destination in the 

world. The primary attraction is the 220-mile long Florida Reef Tract (FRT), the only living coral 

rccf ecosyslem withilt the continental United States, which attracts some 2.5 millioli tourists a year. 

Coral reefs are among the most productive and diverse ecosystems in the world and, as such, are 

co~iiparable to their terrestrial counterparts -- tropical rainforests. Coral reefs grow as a thin veneer 

of living coral tissue on the outside oftlie hermatypic (reef-forming) skeleton and accrete massive 

111nestonc forltiations over geologic time. Coral reefs have evolved over hundreds of ntillions of 

years in tropical and sitbtropical waters that typically have very low concentrations of dissolved 

rnorganic nutrients. Under such conditions, corals recycle limited nutrient supplies via a symbiosis 

In which the host coral releases waste dissolved nutrie~lts that are tightly recycled by the symbiotic 

zooxa~ithellae algae -- which in turn provide carbon-rich conlpounds to the coral. The calcification 

process in corals also generates prorons, which provide for co-transport of nutrients into the corals, 

providing these reef-builders with a competitive advantage over flestly, non-calcareous algae under 

low nutrient conditions. Bccausc ofthe ability ofcorals to thrive in nutrient-poor surface waters of 

tropical oceans, ecologists refer to them as "oases in ocean deserts". 

Scientists have long known that even slight increases in nutrient concentratioits froni sewage 

and other land-based liuman activities can have catastrophic effects on the hcaltli of coral reek. 

Nutrient enrichment increases the growth a~id respiration rate of the nitrogen-limited symbiotic 

zooxa~tthellae, which decreases the photosynthesis to respiration ratio in corals and leads to 

pl.rysiological "stress". Nitrogen-enriched growth of zooxanthellae also alters the biochemistry ofthe 

symbiosis by shifting algal photosynthesis towards production of protein at the expense of 

carbollydrate - undermining the functional nutrition of the symbiosis (ironically, the coral starves 

under high nitrogen coiiditions). Nutrient enrichment can also result in increased cover ofsofi corals 

(non-hcnitatypic), as well as blooms ofmacroalgae (> 2 cni high) and endolithic filamentous algae, 

all of which outco~npete and physically overgrow more slowly growing reef-forming hard corals. 

Elevatcd nutrients reduce overall reef growth by reducing calcification in corals, botli directly and 

indirectly by reducing light and photosynthesis (which is directly linked to calcification) due to 

shading by macroalgae, turf algae, and increased light attenuation of the water colu~nn froni 

increased phytoplankton biomass and turbidity. Nutrient enrichment also leads to increased 
Opporrlcriities artd Cliallengesfir Profectirig, Restorin'ng and Er'rlhariciiig 

Coasral fIabitats in the Bqj of Ftrrtci?, 

abundance of herbivores and corallivores, including parrotfish, sea urchins, and "Crown-of-Thorns" 

starfish that can reduce living coral cover and accelerate bioerosion of limestone reef frameworks. 

Recognition of regional eutrophication in the Florida Keys 

Beginning in tlie late 1970's and early 1980's, hard coral cover began to decline with parallel 

increases in algal turf, macroalgae, and soft corals on patch and bank reefs of the FRT. This biotic 

phase-shificorrelated with increasing human activities and associated nutrient loads from the Florida 

Keys that included deforestation, fertilizer use, sewage inputs, and fossil fuel combustion. In 

addition, a major change in water management policy in South Florida occurred in tlie late 1970's. 

Tliis involved diverting massive flows of stomiwater runoff from the Everglades Agricultural Area 

(EAA) southward towards Everglades National Park (ENP) and Florida Bay, ratiier than 

backpu~iiping into Lake Okeecllobee that was causing hypereutrophication of tlie "Big Lake". 

Scientists documented the impacts oftlle increased nitrogen and phosphorus loads on eutrophicallon 

of the oligotrophic sawgrass and periphyton comniu~lities ofENP as commercial fishermen reported 

the expansion of macroalgae and phytoplankton blooms in seagrass meadows of Florida Bay. 

SCUBA divers on downstream reefs in the Florida Keys reported decreased visibility and tile first 

coral bleaching of the FRT on reefs offshore Key West in summer of 1980. Heavy rains and high 

Everglades flows associated with the 1982-83 El Nino were followed by "wliite band" diseasc that 

cattscd widespread loss of eikhoni (Acroporupulr~~ata) and staghorn (Acropora cer-vicorrris) corals 

while "black band" disease began eroding coral tissue on mountain (Moriiustrea spp.) and brain 

corals (Diploria, Colpop1i)illia). In summer of 1987, a massive die-off of turtle grass (Tlrnlr~ssiu 

res~iirfiniirri) began in central FloridaBay coincident with the first massive coral bleaching throughout 

the FKNMS. 

In response to the deteriorating water quality, loss of coral cover, and ccological problems 

in Florida Bay and tlie Florida Keys, over 50 scientists, educators, and managers attended a NOAA 

sponsored researcli and management workshop in Key Largo in June 1988. Rankiiigs were made by 

the attendees as to tlie major thrcats and problems facing coral reefs of the Florida Keys. Although 

anchor damage by boaters had been considered the primary problem facing coral reefs in the 1970's, 

attendees now concluded that excessive nutrient loading and eutrophication was the top priority issue 

to be addressed to protect the coral reefs: "Excessive nutrients invading the Florida ReefTract from 

the Keys and Florida Bay are a serious and widespread problem" (NOAA 1988). A prirnary conceni 

ofattendees oftliat workshop was whether or not their recommendations would be implemented and 

funded. Widespread attention to the declining status of South Florida's coral reefs occurred in 1990 

whcn Nuriortul Geograpliic featured the article "Florida's Imperiled Coral Reefs" that specifically 

noted tlle growing problcm of nutrient pollution, algal bloon~s, and reef coral die-off. 

The i~iteniational attention to tlie decline of coral reefs in South Florida helped to spur 

passagc of the Florida Keys National Marine Sanctuary (FKNMS) and Protection Act on November 

5,1990, lo "provide long-tern1 protection to the coral reefresources ofthe Florida Iceys". Uniquely, 

thc FKNMS Act includcd an inter-agency (USEPA, NOAA) Water Quality Protection Program 
Opportur~ities artd Cltuller~ges for Protecti~ig, Restoritlg and E~iltuttcir~g 

Couslal Habitats in the Bajl offir~tdy 

(WQPP) intended to protect south Florida's coral reefs from further water quality degradation. The 

WQPP, which was implemented by USEPA, was intended to: 1) develop a monitoring program for 

water quality, coral reef communities, and seagrasses to determine "status and trends" and 2) 

recommend priority corrective actions and compliance schedules addressing point and non-point 

source pollutiori to restore and liiaintain the chemical, physical, and biological integrity of the 

FKNMS. During Phase I ofthe WQPP, information was compiled and syithesized on the status of 

water quality in the FKNMS and Florida Bay. Despite existing scientific kno~vledge of the role of 

nitrogen-rich runoff from the Everglades in fosteringphytoplankton blooms, turbidity, and seagrass 

die-off in Florida Bay, the USEPA Phase 1 Report concluded: "even though the ultimate cause ofthe 

present seagrass die-offhas yet to be proven conclusively, it seems clear that anthropogenic nutrient 

input to the surface water is not responsible" (USEPA 1991). 

While USEPA's Phase 1 Report (1991) categorically dismissed the role of nutrient 

enrichment and eutrophication to the ecological problenis of Florida Bay, the report alteniatively 

promoted the hypothesis that the seagrass die-off resulted from "liypersalinity". The report claimed 

tlrat draining of tlie Everglades caused the diversion of freshwater from Florida Bay, resulting in 

salinities of 55 ppt in central Florida Bay that vvere"fatal" to seagrasses. Act~~ally, the high salinities 

in central Florida Bay referred to in the Phase I Report during the late 1980's were a result of a 

drought wlien South Florida received annual rainfall that was - 30-40 O/o lower than nonnal several 

years in a row. Experimental studies decades earlier by McMillan and Moseley (1 967) showed that 

T. restltdi~t~ort, the seagrass that was dying off, could grow at salinities up to at least 60 ppt, higher 

than the salinity of 55 ppt wliich the Phase I report claimed was "fatal" to seagrasses. Furthcrnrore, 

tlie lone-term studies - of Tabb et a/. f 19621 decades earlier concluded that T. tcsttidir~~r~rt thrives 

under hypersaline conditions in FloridaBay by stating "with marked reduction in salinity beginning 

in the winter of 1957 and ending - in 1960, tlie Tl~alassia underwent decline in size and abundance 

... they did not return in abundance until the drought of 1961-62, reaching peakgrowth and coverage 

in tile spring of 1962. Thus it appears that long periods ofnear or sliglltly above norn~al salinities are 

a requirement for maximuni growth of Tlialassia". 

Politics as usual: go with the flow 

Despite existing knowledge that hypersalinty was not the real problem and-that nitrogen-rich 

runoff from the Everglades was the more likely factor underpinning tlie decline in water quality and 

seagrass die-off in Florida Bay, a political decision \vas made by water managers and cognizant 

government agencies to "restore" Florida Bay by pumping more nitrogen-rich water from the 

Everglades into the bay. Political support for this decision grew from the Everglades Lawsuit (that 

led to the Everglades Forever Act) that recognized phosphorus but not nitrogen pollution of the 

Everglades fro111 the a~cultural activities in the EAA. The Everglades Forever Act called for 

increased flows of low phosphonts water into the Everglades and Florida Bay as the primary basis 

for "Everglades Restoration". Ironically, expensive practices to remove phosphorus in and around 

the EAA by sugarcane farmers and the South Florida Water Management District's (SFWMD) 

"Stormwater Treatment Areas" (STA's) will increase the nitrogen loading to downstream waters of 
Opportu~rities and Cltallet~ges for Profecting, Restoring arrd Ei:liar~cing 

Coastal Habitats in the Bay ofF11t2dy 

the ENP and Florida Bay because of decreased plant growtli and nitrogen removal in the Everglades 

wetlands as a result of greater pitosphorus limitation of plant growth. 

litcreasing Fresh water flows and associated non-point source nitrogen pollution of Florida 

Bay and downstrealn waters of tlte FRT became a "high priority" of tlte FKNMS Management 

Plai~/EnviroitmentaI Inlpact Statement (NOAA 1996). Curiously, while the FKNMS managenlent 

plan promoted policies that increased regional nitrogen pollution from agricultural activities in the 

Everglades, it also gave a "low priority" to monitoring domestic wastewater surface discharges into 

the FKNMS (NOAA 1996). Researcl~ by tlie Florida Department of Environmental Protection and 

other scientists had documented, in great detail, the ecological and public health impacts of sewagedriven eutropltication and bacterial contantination of surface waters of the FKNMS. However, 

cxl~ensivc remedial actions such as Advanced Wastewater Treatment (including nutrient stripping) 

were a volatile and controversial issue in the Keys at that time due, in large part, to a growing lack 

of confidence in the FKNMS process. A referendum vote in Monroe County (Florida Keys) in 1996 

found 54 % ofthe voters against NOAA and the FKNMS Management Plan --although the vote was 

non-binding. The regional eutrophication problem appears to have exacerbated local sewage 

coittamination in the Florida Keys as high fecal coliform counts in the past several years have 

resulted in numerous and extended beach closures f~om Key Largo to Dry Tortugas. 

The lack of confidertce by the local comn~unity in the FKNMS was directly related to tlie 

worsening of regional water quality with implementation of the FKNMS "restoration" plan for 

Florida Bay. The FKNMS management plan was promoted by several national NGO's (Audubon 

Society, Nature Coitservancy, Wildenless Society, Environmental Defense Fund) who joined the 

political bandwagon to "flood tlte bay". Scientific consultants to ENP had misrepresented tltequality 

ofwater flowing through the Everglades as "distilled water"(1annotta 1996) when, in fact, the water 

in Shark River Slough averaged - 100 pM total nitrogen. Beginning in 1991, increased fresltwater 

discharges from both Shark River Slough and Taylor Slough in the ENP (Rudnick et al. 1999) 

correlated significantly with decreased salinity throughout tlie bay and increases in ammonium 

(central bay), phytoplankton biomass (chlorophyll a, western bay), and turbidity (bay-wide, Boyer 

et 01. 1999). Between 1991 and 1996 average salinity in FloridaBaydecreascd f~om 41 ppt to 23 ppt, 

a 44 %decrease in bay-wide salinity. Following the decreased salinity and increase in aninioniunt 

in 1991- 1992, cascading ecological disturbances in the bay included a massivecyanobacterial bloom 

(5j~r1eclrococcus) that was followed by a sponge die-off, hrther seagrass die-off, and the largest red 

tides to ever affect the FKNMS region. 

Analysis of tile Florida Bay data sltows that the developmeitt of phytoplanktoii blooins in 

both the western and central bay followed the increased nitrogen loads and .were most severe in 

central FloridaBay where the ltighest dissolved inorganic nitrogen (DIN) and chloropliyll a occurred. 

This is also the locatioii where the initial scagrass die-off began in 1987. This spatial pattern 

supports the hypothesis that increased ammonium resulting From agricultural activities at the 

headwaters ofboth Shark River Slough and Taylor Slough were tlie primary DIN source (s) fueling 

the phytoplankton blooms in western and central Florida Bay (Lapointe and Clark 1992, Lapointe 
Opportultities atid Cl~alletzges for Protectitig, Restoririg and Etika~~citrg 

et nl. 1993). These phenomena provide strong evidence that nitrogen enrichment, rather than 

hypersalinity, was the more important ecological factor causing the demise of T. tesitrdirlrltl~ in the 

bay. Contrary to the USEPA Phase I Report (1991), a recent NOAA National Estuarine 

Eutrophication Assessment ranked Florida Bay as having a "high" level of expression of eutrophic 

conditions, an index based on chlorophyll a, macroalgal abundance problems, epiphyte abundance 

problems, low dissolved oxygen, nuisance and toxic algal blooms, and loss of submerged aquatic 

vegetation (Brieker ei al. 1999). 

The net cumulative outflows from Florida Bay pass through the tidal channels of the middle 

and lower Florida Keys and flow west-southwest at - 4 cdsec, impinging on the outer bank reefs 

of the FRT. Accordingly, the accelerated eutrophication of Florida Bay in 1991-1992 had 

downstream ecological effects that affected offshore bank reefs of the FRT. A long-tern1 nutrient 

monitoring program at Looe Key National Marine Sanctuary (LKNMS) offshore Big Pine Key 

recorded maximum average concentrations of DIN (> 3 pM) in 1992, whicli coincided with peak 

DIN in central Florida Bay following the "first flush" of Everglades runoff since the drought of the 

late 1980's; this DIN concentrations at LKNMS is quite high compared to the annual nlcan DIN 

concentratio~ts that averaged < 0.6 pM during the decade ofthe 1980's (Lapointe and Matzie 1996). 

Following this regional spike in DIN in 1992, both chlorophyll a and turbidity ofthe water column 

increased at LIWS to maximum values (annual mean chlorophyll a of - 0.6 pdl) in 1996 that 

coincided with peak flows front Shark River Slough. AVHRR satellite images showed very high 

reflectance values associated with the turbid, Florida Bay outflows that moved offshore and over the 

bank reefs, especially during the windy winter and spring months. The deteriorated water quality 

on offshore reefs coincided with an exponential increase in coral "disease" and die-off, reported as 

a 250 %t increase between I996 and 1997 (USEPA 1997). 

Since thc Everglades flush began in 1991-1992, DIN concentrations have averaged > I pM 

at LKNMS, indicating - 100 % increase in biologically available nitrogen at this offshore reef site 

(Lapointe etal. 2000). Bank reefs ofthe FRT had more than 70 %coral cover in the 1970's and now 

average - 15 % coral cover, or less. For example, the shallow fore reef at LKNMS, which was 

historically dominated by Acroporclpal~i~uta and considered one of theKeysl top dive sites, now has 

less than 5 % coral cover. As coral cover has receded, turf algae, macroalgae have increased at 

LKNMS and other offshore reefs, collectively accounting for 48-84 % ofbenthic cover (Chiappone 

and Sullivan 1997). Dawes et al. (1999) recently reported a 67% decrease in macroalgal species 

diversity behveen 1964 and 1996 at the Content Keys in the lower Florida Keys as a result of 

nutrification; as the total number of species declined, nutrient indicator species such as the green 

algae Ulva lactllca and Cl~aeion~orpl~a hracltj~gona appeared. 

Failing the "Everglades Test": what's next ? 

Majorie Stoneman Douglas, life-long advocate and protector of the Everglades' "River of 

Grass", once challenged that "the Everglades is a test; ifwe pass it, we get to keep the planet". Now, 
Opportur~ities and C/~rrllettgesfot Protectiilg, Restori~lg arid E~llrancing 

Coastal Habitats irl the Bay of F~;lrrrdjt 

following a decade of expensive research, monitoring, and management by the FKNMS and 

numerous agencies involved with Everglades Restoration, it is useful to look back and assess what 

went wrong. Despite pre-existing knowledge and scientific consensus of a "serious" regional nutrient 

cnrichnient problem in Florida Bay and the FRT the late 1980's (NOAA 1988), the scientific and 

managentent community in the FKNEvlS process during the 1990's failed to respond in a timely 

manner to develoo a nutrient source identification/evaluation/mitieation . framework. The lack of a 

management framework to address the over-arching regional water quality degradation and mission 

of the FIWMS can be traced to at least four uroblems: I) the lack of technically-trained resource 

managers that understood the basic coastal marine eutrophication problem, especially that in Florida 

Bay, 2) research dominated by marine biologists with reductive and often inaccurate or misleading 

(e.g. "hypersalinity hypothesis") approaches, rather than oceanographers or environmental scientists 

with systems approaches, 3) implementation of a spatially-extensive and expensive water quality 

monitoring program that had inadequate sampling frequency to detect year-to-year clia~iges in even 

the most basic water quality parameters and conducted with no clear idea as to how the data would 

be used; and 4) scientists, managers, and policymakers involved with Everglades and Florida Bay 

"restoration" worked within a framework controlled by "top-down" political forces and land-use 

issues, which undermined a search for "scientific truth" by an otlierwise objective "botto~ii-up" 

approacli (Popper 1994). 

Two critical aspects ofany environmental risk assessment are "getting the right scicncc" and 

"getting the science right". The failure in these two key steps by scientists and managers in South 

Florida during the 1990's were primary factors enabling the protracted time frame in which the 

severe water quality degradation described above has been (and continues to be) neglected. 

Hopefully, this case study will serve to inspire those in other coastal regions, especially in similar 

regions with sensitive coral reef resources, to implement water quality protection policies based on 

good science and aprecautionary management framework. Such an approach will be required if the 

impacts of the escalating trend of nutrient enriclinient to coastal systems is to be moderated. It 

rcniains to bc seen if-adaptive management" can be introduced to the ongoing and expensive (S 7.8 

billion) "Everglades Restoration" plan. Indeed, it would be novel to recognize and manage for 

downstream impacts of land-based nitrogen enricliment in South Florida - a problem recognized 

by oceanographers over I00 years ago (Brandt 1899). 

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Opport~irtities and Cltallenges for Protectiilg, Restorirlg urtd Ei~l~ar~cirtg 

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