Opporturzitiesatid Cl~allerlges for Protecti~lg, Restoring and Enirar~cirlg Coastcrl ifabitatsin theBay 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 ofMarine Sciences, I-IarborBranch 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 rccfecosyslem 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 oftliehermatypic (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 ofnutrients into the corals, providing these reef-builders with a competitiveadvantage over flestly, non-calcareous algaeunder low nutrient conditions. Bccausc oftheability ofcoralsto thrive in nutrient-poor surface waters of tropical oceans, ecologists refer to them as "oases in ocean deserts".

Scientists have longknown that even slightincreases 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 ofzooxanthellae also altersthe 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 underhigh nitrogen coiiditions). Nutrient enrichment can alsoresult in increased coverofsoficorals (non-hcnitatypic), aswell asblooms 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 increasedOpporrlcriitiesartd Cliallengesfir Profectirig,Restorin'ngandEr'rlhariciiig CoasralfIabitats in the Bqj of Ftrrtci?,

abundanceofherbivores and corallivores, including parrotfish, seaurchins, 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 declinewith parallel increases in algal turf, macroalgae, and soft corals on patch and bank reefs ofthe FRT. This biotic phase-shificorrelatedwith increasing human activitiesand 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 impactsoftlle increased nitrogen and phosphorus loadson eutrophicallon ofthe oligotrophic sawgrassandperiphyton comniu~lities ofENPascommercialfishermen 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 centralFloridaBay coincidentwith 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 anchordamageby boaters had been considered the primary problem facing coral reefs in the 1970's, attendeesnowconcluded that excessive nutrient loading and eutrophicationwasthe 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).Aprirnary conceni ofattendeesoftliatworkshop was whether ornot their recommendations would be implemented and funded. Widespread attention to the declining statusofSouth Florida's coral reefs occurred in 1990 whcn Nuriortul Geograpliic featured the article "Florida's Imperiled Coral Reefs" that specifically noted tlle growing problcm ofnutrient 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 ofthe Florida Keys National Marine Sanctuary (FKNMS) and Protection Act onNovember 5,1990, lo "provide long-tern1 protection to the coral reefresources oftheFlorida Iceys". Uniquely, thc FKNMS Act includcd an inter-agency (USEPA, NOAA) Water Quality Protection ProgramOpportur~ities artd Cltuller~ges for Protecti~ig, Restoritlg 

### and E~iltuttcir~g CouslalHabitats 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 oftheWQPP, 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-offin Florida Bay, theUSEPAPhase 1 Report concluded: "even though the ultimate causeofthe present seagrassdie-offhas yet to be proven conclusively, it seemsclear 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-offresulted from "liypersalinity". Thereport claimed tlrat draining of tlie Everglades caused the diversion of freshwater from Florida Bay, resulting in salinities of55 ppt in centralFlorida Baythat vvere"fatal" to seagrasses. Act~~ally, thehigh salinities in central Florida Bay referred to in the Phase 

### I Report during the late 1980's were a result of a drought wlien SouthFlorida 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 (1967) showed that T. restltdi~t~ort, the seagrassthat was dying off, could grow at salinities up to at least 60ppt, 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 19621decades earlier concluded that 

### T. tcsttidir~~r~rt thrives 

## - under hypersaline conditions in FloridaBayby 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 abundanceuntil the drought of 1961-62,reaching peakgrowth and coverage in tile spring of 1962.Thus it appears that longperiods ofnearorsliglltlyabovenorn~al salinities are a requirement for maximuni growth of Tlialassia".

Politics as usual: 

### go with the flow

Despite existingknowledge that hypersalintywasnot thereal problem and-that nitrogen-rich runoff from theEverglades was the more likely factor underpinning tlie decline in water qualityand 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, expensivepractices 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 loadingto downstream waters ofOpportu~rities and Cltallet~ges for Profecting, Restoring 

### arrdEi:liar~cing CoastalHabitats in the Bay ofF11t2dy

the ENP and Florida Baybecause ofdecreased plant growtliand nitrogen removal in the Everglades wetlands as a result of greater pitosphorus limitation ofplant 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 domesticwastewater surface discharges into the FKNMS (NOAA 1996). Researcl~ by tlie Florida Department ofEnvironmental Protection and other scientists had documented, in great detail, the ecological and public health impacts ofsewagedriven eutropltication and bacterial contantination of surface waters of the FKNMS. However, cxl~ensivc remedial actions such as Advanced Wastewater Treatment (includingnutrient stripping)

were a volatile and controversial issue in the Keys at that time due, in large part, to a growing lack ofconfidence in the FKNMS process. Areferendum vote in Monroe County (FloridaKeys) in 1996 found 54 %ofthevoters againstNOAA and the FKNMS Management Plan --althoughthe 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 tltebay". Scientificconsultantsto ENPhad misrepresented tltequality ofwater flowing through theEverglades as "distilled water"(1annotta 1996) when, in fact, the water in Shark River Slough averaged

# - 100pM 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 1996average salinity in FloridaBaydecreascd f~om 41 ppt to 23ppt,

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 centralFloridaBaywheretheltighestdissolved inorganic nitrogen (DIN) and chloropliyll aoccurred. 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

### Opportultitiesatid 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 ofexpression ofeutrophic conditions, an index based on chlorophyll a,macroalgal abundanceproblems, epiphyte abundance problems, low dissolved oxygen, nuisance and toxic algal blooms, and loss of submerged aquatic vegetation (Brieker 

### ei al. 1999).

Thenet cumulative outflows from Florida Bay pass through the tidal channels ofthe 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 ofthe FRT. A long-tern1 nutrient monitoring program at Looe Key National Marine Sanctuary (LKNMS) offshore Big Pine Key recorded maximum average concentrations ofDIN (> 

### 3 pM) in 1992,whicli coincided with peak DIN in central Florida Bay following the "first flush" ofEverglades runoff since the drought ofthe 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 andMatzie 1996). Following this regional spike in DIN in 1992, both chlorophyll a and turbidity ofthewater 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 Bayoutflowsthat moved offshore and overthe bank reefs, especially during the windy winter and spring months. The deteriorated water quality on offshorereefs coincided with an exponential increase in coral "disease" and die-off, reported as

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

Sincethc Everglades flush began in 1991-1992, DIN concentrationshave averaged > I pM at LKNMS, indicating

# - 100 % increase in biologically available nitrogen at this offshore reef site (Lapointe 

### etal.2000). Bank reefsoftheFRT had more than 70 %coralcover 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 oneoftheKeysl top dive sites,now has less than 5 % coral cover. As coral cover has receded, turf algae, macroalgae have increased at LKNMS and other offshorereefs, collectively accounting for48-84 %ofbenthiccover (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 ofthe Everglades' "River of Grass", oncechallenged that "the Everglades is a test; ifwepass it, we getto keep theplanet". Now,Opportur~ities and C/~rrllettgesfot Protectiilg, Restori~lg arid E~llrancing Coastal Habitats irl theBay ofF~;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 consensusofa "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-archingregional water quality degradation and mission of the FIWMS can be traced to at least four uroblems: I) the lack of technically-trained resource managersthat 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 orenvironmental 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 qualityparameters and conducted with no clear idea asto 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).

Twocritical aspects ofanyenvironmental 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 qualityprotection policies based on good scienceand 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 

### (S7.8 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).

References

Brandt, I<. 1899. Ueber den Stoffweclisel im Meeere. Rede beim Antritt des Rektorates dcrIConigliclien

### Christian-Albreehts-Universilatzu Kicl am

### 6.Marz 1899.Kiel: UniversitatsBt~clihandlung, 36 pp.
Boyer, J.N., J.W. Fourqurean arid R.D. Jones. 1999. Seasonal and long-term trends in the water quality of Florida Bay (1989-1997). Estuaries 22: 412-430.Opportlcitities at~d Cllaller~ges for Protecting, Restorirtg attdEttlzarlcing CoastalIfibitats itr iheBay ofFici14)j

Bricker, S.B., C.C. Clement, D.E. Pirhalla, S.P. Orlando and D.R.G. Farrow. 1999. National Estuarine Eutrophication Assessment: Effects of Nutrient Enrichmerit in tlie Nation's Estuaries. National Oceans Studies Special Projects Office, National Oceanic and Atmospheric Administration, Silver Springs, MD.

Cliiapponc, M.and K.M. Sullivan. 1997.Rapid assessment ofreefsinthe Florida Keys: results from a synoptic sunley. Proc. 8"' International Coral Reef Syinposiu~n 2: 1509-1514.

Dawcs, C.J., C. Uranowski, J. Andorfer and B. Teasdale. 1999. Changes in the macroalga taxa and zonation at tlie Content Keys, Florida. Bulletin ofMarine Science 64: 95-102.

lannotta, B. 1996. Mystery of the Everglades. New Scientist 2055: 35-37.

Lapointe, B.E. and M.W. Clark. 1992.Nutrient inputsfrom thewatershed and coastal eutrophication in the Florida Keys. Estuaries 15:465-476.

Lapointe, B.E., W.R. Matzie and M.W. Clark. 1993. Phosphorus inputs and eutrophicatio~i on tlie Florida Reef Tract. In: Global Coral Reefs: Health, Hazards and History, University of Miami.

Lapointe, B.E. and W.R. Matzie. 1996. Effects of stomiwaternutrient dischargeson eutropllication processes in nearshore waters of the Florida Keys. Estuaries 19: 422-435.

Lapointe, B.E., C.S. Yentsclt, C.M. Yentsch, P. Barile, D. Piiinney, 

### J. Vanderbloemen and S. Andrefouet. 2000. Decadal scale nutrient enrichment correlates with changes in the optical properties and biotic structureofcoral reef coriimunities on bank reefs of the lower Florida Keys. Proc. 9"' Int. Coral Rcef Syiiiposium, Bali (in press).

McMillan, C. and F.N. Moseley. 1967.Salinitytolerances offive marine spemiatophytes ofRedfish Bay, Texas. Ecology 48: 503-506.

NOAA. 1988. Results of a workstlop on coral reef research and management in the Florida Keys: a blueprint for action. In: J. Miller (Ed.). Technical Report, National Underseas Research Program, Washington, DC.

NOAA. 1996. Strategy for Stewardship: Florida Keys National Marine Sanctuary: Final Management Plan~Enviro~irrierital Inipact Statement. VolumeI, OfficeofOcean and Coastal Resource Management, Sanctuaries and Resenres Division, Washington, DC, 319 pp.
Popper, K.R. 199-1. The myth of the framework. I11 dcfencc of science and rationality. Routledge, New York, 230 pp.Opport~irtities and Cltallenges for Protectiilg,Restorirlg urtd Ei~l~ar~cirtg Coastal Habitats in theBay 

### ofFt~nd)r

Rudnick, D.T., 2. Chen, D.L. Childers, J.N. Boyer and T.D. Fontaine. 1999. Phosphorus and nitrogen inputs to Florida Bay: the intportance of the Everglades watershed. Estuaries 22: 398-416.

Tabb, D.C., D.L. Dubrow and R.B. Manning. 1962. The ecology of northern Florida Bay and adjacent estuaries. State of Florida Board of Conservation, Technical series No. 39, The Marine Laboratory, University ofMiami, FL.

USEPA. 1991.Water Quality Protection Program forthe Florida Keys National Marine Sanctuary: Phase I Report. Office of Wetlands, Oceans, and Watersheds, Wasltington, DC.

USEI'A. 1997. Water Quality

### Protection Prograin forthe Florida Keys National Marine Sanctuary: Coral ReerMonitoring Program, Press Release.