ArticlePDF Available

Macroalgal blooms on southeast Florida coral reefs: I. Nutrient stoichiometry of the invasive green alga Codium isthmocladum in the wider Caribbean indicates nutrient enrichment


Abstract and Figures

Invasive blooms of the siphonaceous green algae Codium spp. have been considered a symptom of coastal eutrophication but, to date, only limited biochemical evidence supports a linkage to land-based nutrient pollution. Beginning in the summer of 1990, spectacular blooms of unattached Codium isthmocladum developed on deep coral reef habitats in southern Palm Beach County and northern Broward County, and in subsequent years, attached populations formed on reefs in northern Palm Beach County.To better understand the nutrition of these HABs, we collected C. isthmocladum and other reef macroalgae from various locations in southeast Florida as well as the wider Caribbean region for tissue C:N:P analysis in order to gauge variability in the type and degree of N- and/or P-limited growth. Widespread nutrient enrichment in floridian C. isthmocladum populations was evidenced by significantly higher tissue P (0.06% versus 0.04% of dry weight) and lower C:N (12 versus 19), C:P (425 versus 980), and N:P (35 versus 50) ratios compared to more nutrient-depleted Caribbean populations. To determine nutrient availability on southeast Florida's reefs, we sampled near-bottom waters at a variety of locations for DIN (NH4+ + NO3− + NO2−) and SRP analysis. In general, concentrations of NH4+, NO3− and SRP were all high on southeast Florida's reefs compared to values reported for Caribbean coral reefs. Although summertime upwelling provides episodic NO3− and SRP enrichment to reefs in southeast Florida, these transient nutrient pulses have not historically supported C. isthmocladum blooms.We suggest that the widespread P enrichment of C. isthmocladum tissue and water column DIN:SRP ratios <16:1 in southeast Florida drive this system toward N limitation where low level NH4+ enrichment becomes of paramount importance. Hence, the recent C. isthmocladum blooms appear to be supported by increasing land-based nutrient pollution, particularly, sewage that is enriched in NH4+ and SRP at a low N:P ratio (<10:1) critical to sustaining balanced growth during bloom formation.
Content may be subject to copyright.
Macroalgal blooms on southeast Florida coral reefs
I. Nutrient stoichiometry of the invasive green alga
Codium isthmocladum in the wider Caribbean
indicates nutrient enrichment
Brian E. Lapointe
*, Peter J. Barile
, Mark M. Littler
Diane S. Littler
, Bradley J. Bedford
, Constance Gasque
Harbor Branch Oceanographic Institution, Inc., 5600 US 1 North, Ft. Pierce, FL 34946, USA
Department of Botany, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560, USA
Department of Environmental Sciences, Florida Atlantic University, Boca Raton, FL 33431, USA
Received 30 November 2004; received in revised form 1 June 2005; accepted 5 June 2005
Invasive blooms of the siphonaceous green algae Codium spp. have been considered a symptom of coastal eutrophication but,
to date, only limited biochemical evidence supports a linkage to land-based nutrient pollution. Beginning in the summer of 1990,
spectacular blooms of unattached Codium isthmocladum developed on deep coral reef habitats in southern Palm Beach County
and northern Broward County, and in subsequent years, attached populations formed on reefs in northern Palm Beach County.
To better understand the nutrition of these HABs, we collected C. isthmocladum and other reef macroalgae from various
locations in southeast Florida as well as the wider Caribbean region for tissue C:N:P analysis in order to gauge variability in the
type and degree of N- and/or P-limited growth. Widespread nutrient enrichment in floridian C. isthmocladum populations was
evidenced by significantly higher tissue P (0.06% versus 0.04% of dry weight) and lower C:N (12 versus 19), C:P (425 versus
980), and N:P (35 versus 50) ratios compared to more nutrient-depleted Caribbean populations. To determine nutrient
availability on southeast Florida’s reefs, we sampled near-bottom waters at a variety of locations for DIN
) and SRP analysis. In general, concentrations of NH
and SRP were all high on southeast
Florida’s reefs compared to values reported for Caribbean coral reefs. Although summertime upwelling provides episodic NO
and SRP enrichment to reefs in southeast Florida, these transient nutrient pulses have not historically supported C. isthmocladum
We suggest that the widespread P enrichment of C. isthmocladum tissue and water column DIN:SRP ratios <16:1 in
southeast Florida drive this system toward N limitation where low level NH
enrichment becomes of paramount importance.
Hence, the recent C. isthmocladum blooms appear to be supported by increasing land-based nutrient pollution, particularly,
Harmful Algae 4 (2005) 1092–1105
DOI of original article: 10.1016/j.hal.2005.06.002.
* Corresponding author. Tel.: +1 772 465 2400x276; fax: +1 772 465 0134.
E-mail address: (B.E. Lapointe).
1568-9883/$ – see front matter #2005 Published by Elsevier B.V.
sewage that is enriched in NH
and SRP at a low N:P ratio (<10:1) critical to sustaining balanced growth during bloom
#2005 Published by Elsevier B.V.
Keywords: Nitrogen; Phosphorus; Macroalgae; Coral reefs; Eutrophication
1. Introduction
Coral reef ecosystems are adapted to oligotrophic
tropical and subtropical waters and are sensitive to low
level increases in the concentrations of dissolved
inorganic nitrogen (DIN) and soluble reactive phos-
phorus (SRP) associated with cultural eutrophication
(Johannes, 1975; Tomascik and Sander, 1987; Bell,
1992; NRC, 1995; Dubinsky and Stambler, 1996).
Nutrient enrichment of coral reefs has many direct and
indirect effects that, over time, can result in an
alternative stable state dominated by fleshy, non-
calcifying macroalgae (Birkeland, 1987; Done, 1992;
Lapointe et al., 1993, 1997; Lapointe, 1997; NRC,
2000; Bellwood et al., 2004). Growth and reproduc-
tion of macroalgae are nutrient limited in oligotrophic
coral reef waters (Lapointe, 1987, 1997, 1999; Larned
and Stimson, 1996; Schaffelke and Klumpp, 1998;
Lapointe et al., 2004) where low nutrient concentra-
tions and high turbulence favors the dominance of
calcifying, hermatypic corals (Adey, 1998; McCon-
naughey et al., 2000). Case studies in Kaneohe Bay,
HI, USA (Banner, 1974; Smith et al., 1981), and more
recently, the Negril Marine Park, Jamaica (Lapointe
and Thacker, 2002) have demonstrated the pivotal role
of low level nutrient enrichment to the development of
excessive macroalgal biomass—harmful algal blooms
(HABs; ECOHAB, 1997)—on coral reefs. Macroalgal
HABs can inhibit the survival of coral recruits
(Birkeland, 1977; Sammarco, 1980, 1982) and
because of enhanced growth and reproduction in the
presence of elevated nutrients, macroalgae can quickly
overgrow and replace the slower growing reef-forming
(hermatypic) corals (NRC, 1995). Additionally,
increases in macroalgal biomass typically result in
elevated sea urchin densities and the subsequent
bioerosion of reefs (Sammarco, 1982; Lapointe and
Thacker, 2002).
Macroalgal HABs have developed in many
tropical/subtropical coral reef communities in recent
decades as a result of increasing land-based nutrient
pollution (UNEP, 1994; ECOHAB, 1997; NRC,
2000). During the summer of 1990, coral reefs off
southern Palm Beach and northern Broward counties
in southeast Florida experienced an unprecedented
succession of macroalgal blooms first evidenced by
unattached populations of the green alga Codium
isthmocladum on deep (>30 m) reefs. Historically,
C. isthmocladum occurred at low standing crops in
these deep reef communities (24–58 m) in the 1970s
(Hanisak and Blair, 1988). However, the more recent
blooms resulted in biomass accumulations up to 2 m
thick over the reef surface, which resulted in an
emigration of reef fish populations from the
impacted areas and die-offs of sponges, hard corals
and soft corals via physical smothering and hypoxia/
anoxia (Lapointe, 1997; Lapointe and Hanisak,
1997). By the mid-1990s, blooms of attached
populations of C. isthmocladum spread to reefs in
northern Palm Beach County, which were followed
by extensive blooms of Caulerpa spp. (see Lapointe
et al., 2005).
Species in the green algal genus Codium are widely
known as invaders of coastal waters (Ramus, 1971;
Fralick and Mathieson, 1973; Carlton and Scanlon,
1985; Trowbridge, 1998) and their abundance in
certain tropical/subtropical habitats also suggests they
may be ecological indicators of nutrient enrichment.
Blooms of invasive Codium fragile occurred in the
northwestern (Fralick and Mathieson, 1973; Carlton
and Scanlon, 1985) and northeastern (Silva, 1957)
Atlantic decades ago. In the Niantic River estuary, CT,
USA, the invasion of C. fragile was related to DIN
availability (Malinowski and Ramus, 1973), although
no evidence of anthropogenic nutrient sources was
reported. Whereas Codium spp. are not conspicuous in
oligotrophic coral reef communities in the wider
Caribbean region (Littler and Littler, 2000), they
commonly form blooms in nutrient replete habitats.
For example, in guano enriched waters surrounding
White Cay north of San Salvador, Bahamas, C.
isthmocladum formed extensive populations in a
B.E. Lapointe et al. / Harmful Algae 4 (2005) 1092–1105 1093
nutrient enriched inner zone around the small island
(Urnezis, 1995). A human induced simulation of this
enrichment effect followed the maritime shipwreck of
the Arimora and its cargo of fertilizer (guano) off Egg
Island near Spanish Wells, Bahamas. Downstream of
the wreck, a halo of macroalgae developed that
included C. isthmocladum (Lapointe et al., 1992).
Both natural and anthropogenic nutrient sources
may be important to C. isthmocladum blooms on reefs
in southeast Florida. Episodic summertime upwelling
has historically occurred in this area (Green, 1944;
Taylor and Stewart, 1958) but, because these HABs
developed only recently, we hypothesized that land-
based nutrient enrichment resulting from increasing
urbanization and associated nutrient pollution from
the watershed is a significant factor. The human
population in the southeast Florida area is now 7
million, with over 12,000 metric tonnes/year of
sewage nitrogen discharged directly into coastal
waters from six ocean outfalls between Dade and
Palm Beach counties (see Lapointe et al., 2005). In
addition, Palm Beach and Broward counties have an
estimated 183,645 septic tanks (
and nearly 30 Class I injection well facilities that
dispose of secondarily treated wastewater under
pressure to depths of 1100 m (USEPA, 2003).
Land-based sewage effluent and stormwater runoff
can enter coastal waters either via submarine
groundwater discharges (SGD, Finkl and Charlier,
2003) or surface water discharges via the Port
Everglades, Hillsboro, Boynton, Lake Worth, and
Jupiter inlets.
To better understand the nutritional status of the
summertime C. isthmocladum blooms, we performed
tissue carbon (C), nitrogen (N), and phosphorus (P)
analyses on C. isthmocladum populations and other
abundant taxa from a variety of reef sites off southeast
Florida to compare with those of C. isthmocladum
populations collected around the wider Caribbean
region. We used this information to gauge the type and
degree of N-limited versus P-limited growth of the
Florida HABs relative to Caribbean populations and to
quantify any effects of anthropogenic nutrient
enrichment on C:N:P contents and molar ratios of
C. isthmocladum tissue. In addition, we collected
near-bottom water samples to determine the avail-
ability of DIN and SRP to these HABs at a variety of
sites on southeast Florida’s reefs.
2. Materials and methods
2.1. Collection sites for C:N:P analysis of
macroalgae: 1994–1998
To assess variability in tissue C:N:P ratios of C.
isthmocladum over the wider Caribbean region
(Fig. 1), we collected plants by SCUBA from a
variety of reef sites in depths of 15–40 m in the
Greater Antilles (Isla de Culebra, PR; Dominican
Republic; Discovery Bay, Jamaica) and Lesser
Antilles (Bird Island, Antigua; Prickley Pear Cays,
St. Martin; Point Perces, Guadaloupe; Ile Perle,
Martinique; Diamond Rock, Martinique; Dark Head,
St. Vincent) in May/June of 1995 and 1996 during
research cruises aboard the R/V Sea Diver. Additional
collections of C. isthmocladum were made on reefs in
the Abacos, Bahamas (Powell Cay, Munjack Cay; 7–
10 m depths) in July of 1995 and at several locations in
the Negril Marine Park, Jamaica (Little Bay,
Ironshore, South Negril, and Davis Cove, 5–23 m
depths; Lapointe and Thacker, 2002) during 1998.
In southeast Florida, C. isthmocladum was collected
for C:N:P analysis between 1994 and 1996 on reefs in
Palm Beach and Broward counties (26–43 m depths;
Lapointe and Hanisak, 1997). We collected C. isthmo-
cladum tissue from four sites in Palm Beach and Martin
counties in August 1994 (Princess Anne, North
Colonel’s Ledge, Jupiter Ledge, Hobe Sound; Lapointe,
1997); from Jupiter Ledge, off northern Palm Beach
County, monthly between May and August, 1995; and
from several sites in northern Broward (Deerfield Reef)
and Palm Beach counties (Jupiter Ledge, Hopper Barge,
Hole in the Wall, North Colonel’s Ledge, Spadefish
Point, Juno Ball, South Double Ledges, Princess Anne,
Boca Raton near the sewage outfall, and Spanish River
Reef) between June and August, 1996. In addition, other
abundant macroalgae (Chlorophyta, Rhodophyta, and
Phaeophyta) were collected from several reef sites in
Broward and Palm Beach counties in 1996 and analyzed
to allow broader assessments of phylogenetic variability
in C:N:P contents.
2.2. Analysis of macroalgae for C:N:P
The collections of macroalgae were processed and
analyzed for tissue C:N:P contents. The Caribbean
samples (Fig. 1) were prepared aboard the R/V Sea
B.E. Lapointe et al. / Harmful Algae 4 (2005) 1092–11051094
Diver, whereas the Florida samples were processed in
the Marine Nutrient Dynamics Laboratory at HBOI in
Ft Pierce, FL. In both cases, composite samples (thalli
from five to eight different plants) of freshly collected
macroalgae were immediately sorted, cleaned of
visible epiphytes and sediments, and rinsed briefly
(3–5 s) in deionized water to remove salt and debris.
The cleaned, composite samples were dried in a Fisher
Scientific Isotemp
oven at 65 8C for 48 h. The dried
macroalgae were ground to a fine powder using a
mortar and pestle and stored in plastic vials in a
dessicator. Samples of the dried, powdered macro-
algae were analyzed for C:N:P contents at the Nutrient
Analytical Services Laboratory, University of Mary-
land, Solomons, MD. Tissue C and N were measured
on an Exeter Analytical, Inc. (EAI) CE-440 Elemental
Analyzer, whereas P was measured following the
methodology of Asplia et al. (1976) using a Technicon
Autoanalyzer II with a IBM compatible Labtronics
Inc. DP500 software data collection system (D’Elia
et al., 1997).
2.3. Seawater nutrient analyses
To quantify DIN ( NH
-N + NO
-N + NO
and SRP (PO
-P) availability on southeast Florida’s
reefs, SCUBA divers collected near-bottom water
samples for low level nutrient analysis from a variety
of reef sites in Palm Beach and Broward counties in
summer 1996 (June–August). Replicate (n= 3–6)
water samples were collected by divers from the
near-bottom layer (5 cm above reef surface) into
clean, HDPE bottles. The water samples were held on
ice in a cooler and subsequently filtered through a
Gelman 0.45 mm GF/F filter and frozen until analysis.
Within 28 days of collection, the samples were
analyzed for NH
-N, NO
-N, NO
-N, and PO
P on either a Bran and Luebbe TRAACS 2000
B.E. Lapointe et al. / Harmful Algae 4 (2005) 1092–1105 1095
Fig. 1. Map showing location of study sites in the wider Caribbean region and southeast Florida (inset).
B.E. Lapointe et al. / Harmful Algae 4 (2005) 1092–11051096
Table 1
Tissue levels (% dry wt.) of carbon (C), nitrogen (N), phosphorus (P), and C:N, C:P, and N:P molar ratios of Codium isthmocladum from
southeast Florida and the wider Caribbean
Location Site Date %C %N %P C:N C:P N:P
Martin Co. Hobe Sound 8/7/94 11.71 1.07 0.06 13 503 39
Palm Beach Co. Jupiter Ledge 8/7/94 11.93 1.00 0.05 14 615 44
5/29/95 10.50 0.57 0.05 21 542 25
6/30/95 6.03 0.52 0.03 14 518 38
7/27/95 10.30 0.72 0.03 17 885 53
8/12/95 9.65 0.74 0.04 15 622 41
8/16/96 10.80 1.23 0.07 10 398 39
Hole in the Wall 7/15/96 8.34 1.44 0.11 7 196 29
Spadefish Point 7/15/96 8.85 1.01 0.07 10 326 32
Juno Ball 7/21/96 9.59 0.77 0.05 15 495 34
N. Colonel’s Ledge 8/7/94 9.74 1.06 0.07 11 359 33
8/16/96 10.70 1.11 0.15 11 184 16
Princess Anne 8/7/94 10.68 0.97 0.06 13 459 36
6/18/96 9.21 1.12 0.08 10 297 31
7/20/96 10.90 1.10 0.07 12 402 35
S. Double Ledges 7/21/96 9.45 0.85 0.06 13 406 31
Boca Raton Outfall 8/27/96 8.79 1.17 0.06 9 378 43
Broward Co. Deerfield Reef 8/27/96 12.00 1.33 0.07 11 442 42
Florida mean 1S.D. 9.95
Puerto Rico Isla de Culebra 6/2/95 12.90 0.74 0.03 20 1109 55
St. Martin Prickly Pear Cays 6/6/95 17.00 0.61 0.09 33 487 15
Antigua Bird Island 6/9/95 14.90 0.91 0.04 19 961 50
Guadeloupe Pointe Perces 6/11/95 12.60 0.64 0.04 23 812 35
Martinique Rocher de la Perle 1 6/13/95 13.50 1.01 0.06 16 580 37
Rocher de la Perle 2 6/13/95 12.30 0.78 0.05 18 634 34
Rocher du Diamant 6/15/95 10.60 0.72 0.05 17 547 32
Little St. Vincent Dark Head 6/19/95 15.00 0.99 0.05 18 774 44
Powell Cay Powell Channel 1 7/4/95 16.00 0.95 0.04 20 1032 53
Powell Channel 2 7/4/95 12.70 0.60 0.02 25 1638 66
Munjack Cay Munjack Cave 1 7/5/95 16.10 1.02 0.03 18 1384 75
Munjack Cave 2 7/6/95 13.60 1.06 0.04 15 877 59
Munjack Reef 1 7/7/95 15.10 1.04 0.03 17 1298 77
Munjack Reef 2 7/7/95 14.80 1.06 0.03 16 1272 78
Dominican Rep. St. Cruz de Barahona 5/30/96 14.30 0.49 0.03 34 1229 36
Jamaica Discovery Bay 6/2/96 14.47 0.88 0.04 19 933 49
Davis Cove, Deep 8/98 15.60 0.80 0.04 23 1006 44
South Negril, Deep 8/98 16.30 1.02 0.05 19 841 45
Ironshore 8/98 17.40 1.18 0.05 17 897 52
Little Bay, Shallow 8/98 21.20 1.26 0.04 20 1367 70
Little Bay. Deep 8/98 15.70 0.76 0.03 24 1350 56
Caribbean Mean 1S.D. 14.86
Grand Mean 1S.D. 12.60
B.E. Lapointe et al. / Harmful Algae 4 (2005) 1092–1105 1097
Table 2
Tissue levels (% dry wt.) of carbon (C), nitrogen (N), and phosphorus (P), and C:N, C:P, and N:P molar ratios in macroalgae from southeast
Phylum Site Date Species %C %N %P C:N C:P N:P
Chlorophyta Jupiter Ledge 8/16/96 Codium isthmocladum 10.80 1.23 0.07 10 398 39
Hole in the Wall 7/15/96 Anadyomene stellata 23.30 2.38 0.14 11 429 38
Codium decorticatum 6.09 0.66 0.07 11 224 21
Codium isthmocladum 8.34 1.44 0.11 7 196 29
Codium repens 11.60 1.34 0.07 10 427 42
Ulva lactuca 20.20 2.26 0.10 10 521 50
Spadefish Point 7/15/96 Anadyomene stellata 21.70 1.78 0.10 14 560 39
Codium isthmocladum 8.85 1.01 0.07 10 326 32
Juno Ball 7/21/96 Codium isthmocladum 9.59 0.77 0.05 15 495 34
Codium repens 12.00 0.94 0.06 15 516 35
N. Colonel’s Ledge 8/16/96 Codium isthmocladum 10.70 1.11 0.15 11 184 16
Princess Anne 6/18/96 Codium isthmocladum 9.21 1.12 0.08 10 297 31
Ulva lactuca 18.70 1.96 0.10 11 482 43
7/20/96 Codium isthmocladum 11.10 1.09 0.07 12 409 34
Codium isthmocladum 10.70 1.11 0.06 11 460 41
S. Double Ledge 7/21/96 Codium decorticatum 8.48 0.66 0.05 15 437 29
Codium isthmocladum 9.45 0.85 0.06 13 406 31
Codium repens 9.18 0.65 0.05 16 473 29
Hopper Barge 8/16/96 Codium decorticatum 9.03 1.11 0.10 9 233 25
Boca Raton Outfall 8/27/96 Codium isthmocladum 8.79 1.17 0.06 9 378 43
Caulerpa racemosa 14.30 1.55 0.07 11 527 49
Deerfield Reef 8/15/96 Codium isthmocladum 10.20 1.23 0.06 10 438 45
8/27/96 Codium isthmocladum 12.00 1.33 0.07 11 442 42
mean 1 S.D.
Rhodophyta Hole in the Wall 7/15/96 Chrysymenia sp. 6.18 0.98 0.08 7 199 27
Gracilaria mammalaris 18.70 2.21 0.15 10 321 33
Halymenia floridana 11.20 1.26 0.08 10 361 35
Scinaia complanata 7.22 1.48 0.13 6 143 25
Spadefish Point 7/15/96 Chrysymenia sp 8.43 1.02 0.07 11 224 21
S. Double Ledge 7/21/96 Botryocladia occidentalis 10.70 1.24 0.12 10 230 23
Bryothamnion sp. 19.20 2.00 0.13 11 381 34
Chrysymenia sp. 3.09 0.30 0.03 12 266 22
Halymenia floridana 11.10 0.88 0.06 15 477 32
Spanish River 8/15/96 Grateloupia sp. 13.80 1.14 0.10 14 356 25
Halymenia floresia 8.96 0.89 0.06 12 385 33
Boca Raton Outfall 8/27/96 Halymenia floridana 11.70 1.44 0.10 9 302 32
Deerfield Reef 8/15/96 Grateloupia sp. 13.40 1.03 0.09 15 384 25
Halymenia floresia 10.80 1.18 0.08 11 348 33
Mean 1 S.D.
Phaeophyta Hole in the Wall 7/15/96 Stypopodium zonale 20.0 1.50 0.08 16 645 41
Spadefish Point 7/15/96 Dictyota divaricata 19.30 1.68 0.13 13 383 29
Stypopodium zonale 26.90 1.64 0.07 19 991 52
Juno Ball 7/21/96 Lobophora variagata 34.80 1.50 0.09 27 997 37
Stypopodium zonale 28.30 1.65 0.07 20 1043 52
Mean 1 S.D.
Mean 1 S.D.
Analytical Console or an Alpkem nutrient autoanalyzer
at the HBOI Environmental Laboratory (HBEL) in Ft.
Pierce, FL. The analytical detection limits for these
analyses were 0.08 mMforNH
, and 0.009 mMforSRP.
The methods for collection, handling, and processing of
the water samples for low level nutrient analysis
followed a quality assurance/quality control protocol
designed to prevent problems associated with sample
contamination and excessive holding times in order to
provide accurate and reliable data (Gunsalus, 1997).
2.4. Statistical analyses
Analysis of tissue C:N:P contents between the
Caribbean region and southeast Florida and nutrient
data from southeast Florida involved both parametric
(ANOVA) and non-parametric tests. We utilized non-
parametric tests (e.g., Kruskall–Wallis H-test, Mann–
Whitney U-test) when assumptions of homogeneity of
variance and sample distribution normality were not
met. Summary statistics are provided in the results
below; reports of significance imply that the prob-
ability of the null hypothesis ( p)is<0.05.
3. Results
3.1. C:N:P analyses of macroalgae
The mean tissue C:N:P composition of C. isthmo-
cladum sampled from reefs in southeast Florida in 1996
was markedly different than in populations from the
Bahamas, Greater Antilles, and Lesser Antilles
sampled between 1995 and 1998 (Table 1;Fig. 2).
Although the mean %N of C. isthmocladum from
southeast Florida (0.99 0.25) was statistically similar
(Mann–Whitney, p= 0.179) to that from the wider
Caribbean region (0.89 0.21), the mean %P of the
Florida populations (0.06 0.03) was significantly
higher than the Caribbean populations (0.04 0.01;
Mann–Whitney, p<0.001). The floridian C. isthmo-
cladum population had lower %C (9.83 1.56 versus
14.83 2.21; p<0.001), C:N (12.22 3.07 versus
19.15 5.21; p<0.001), C:P (425 146 versus
980 278; p<0.001), and N:P ratios (35.0 8.2
versus 50.1 15.0; p<0.001) compared to the
Caribbean populations (Table 1). These regional
differences become even more apparent when urba-
nized sites from the Caribbean (e.g., sites around Forte-
de-France, Martinique; see Littler et al., 1993) are
removed from the comparison (Fig. 2).
Significant phylogenetic differences in mean C:N:P
composition among species of Chlorophyta, Rhodo-
phyta and Phaeophyta were detected (Kruskall–Wallis
test) on reefs in southeast Florida in 1996 (Table 2).
Although the overall mean %P of the three groups
were statistically similar ( p= 0.267), significant
differences were observed for %C (Kruskall–Wallis,
p= 0.003), C:N ( p= 0.004), C:P ( p= 0.001), and N:P
(p= 0.008). Differences in %N were only marginally
significant ( p= 0.063). With the exception of %P,
which was similar among the three phyla, most of the
significant differences in other tissue variables resulted
B.E. Lapointe et al. / Harmful Algae 4 (2005) 1092–11051098
Fig. 2. Tissue carbon:nitrogen (C:N), carbon:phosphorus (C:P), and
N:P molar ratios of Codium isthmocladum at sites in southeast
Florida vs. the wider Caribbean region (locations sampled near
urbanized areas of the Caribbean are omitted from this plot). Values
represent means S.D. (n= 3–12).
from large differences between species of Phaeophyta
and the Chlorophyta/Rhodophyta. For example, the
mean %C was over two-fold higher in the Phaeophyta
(25.86 5.73) compared to either the Chlorophyta
(11.93 4.5) or Rhodophyta (11.03 4.24). Like-
wise, differences between the Phaeophyta and the
Chlorophyta/Rhodophyta occurred for %N (1.59
0.08 versus 1.25 0.46/1.22 0.46), C:N (19.0
4.69 versus 11.4 2.22/10.9 2.55), C:P (812 258
versus 403 107/313 87), and N:P ratios (42.2
8.89 versus 35.5 8.41/28.6 4.82).
3.2. Water column nutrient concentrations
Concentrations of NO
and NH
in near-bottom
reef waters in Palm Beach and Broward counties
ranged from 0.07 to 8.91 mM and from undetectable
(<0.05 mM) to 2.99 mM, respectively, between June
and August 1996 (Fig. 3). The highest NH
trations occurred on shallow reefs (e.g., 4 m, Lake
Worth Pier, Fig. 3) compared to the highest NO
concentrations that occurred on the deepest reefs
during upwelling events (e.g., August 1996 at Hole in
the Wall, North Colonel’s Ledge, Spanish River,
Fig. 3). This depth-related pattern was apparent in
August 1996 off Spanish River (Boca Raton) during an
upwelling event when NO
concentrations increased
with increasing depth; whereas, NH
decreased with increasing depth (Fig. 4A and B).
Significant differences occurred in mean DIN
concentrations between the northern and southern
regions of the study area during summer 1996. Overall,
DIN concentrations were significantly (ANOVA,
F= 9.01, p= 0.0073) greater in the southern (5.22
0.48 mM) compared to the northern region (3.23
0.35 mM, Fig. 3). This difference was largely the result
B.E. Lapointe et al. / Harmful Algae 4 (2005) 1092–1105 1099
Fig. 3. Concentrations (mM) of dissolved inorganic nitrogen (DIN),
soluble reactive phosphorus (SRP), and the DIN:SRP ratio for north
vs. south regions of the southeast Florida study area from June to
August of 1996. Values represent means S.D. (n= 3–6).
Fig. 4. Regressions for: (A) dissolved inorganic nitrogen
-N + NO
-N + NO
-N) concentrations (mM) vs.
depth (m), and (B) NO
concentrations (mM) vs. depth (m).
Samples were collected from reefs off Spanish River, Boca Raton,
August 15, 1996.
of higher concentrations of NO
(ANOVA, F= 13.92,
p= 0.0014) in the southern compared to the northern
region during the 1996 sampling. Concentrations of
were not significantly ( p>0.05) different
between the two regions and averaged 0.82 mM
throughout the study area.
SRP concentrations ranged from 0.066 to 0.766 mM
during the summer 1996 sampling with the highest
concentrations at the site nearest the Boca Raton
sewage outfall (Fig. 3). The mean SRP concentration in
the northern region (0.35 0.05 mM) was lower, but
not significantly ( p>0.05) different than that of the
southern region (0.48 0.07 mM; Fig. 2). The
DIN:SRP ratio averaged 15.3 in the northern region
and 14.4 in the southern region with peak values >20
associated with low SRP concentrations (Fig. 3).
4. Discussion
4.1. Importance of P-availability to bloom
development and species composition
Our comparative studies of C:N:P contents in C.
isthmocladum among a broad spectrum of sites support
previous findings (Lapointe, 1997) of reduced P
limitation in coastal waters of southeast Florida
compared to stronger P limitation in carbonate-rich
Caribbean waters. Lapointe et al. (1992) sampled a
wide variety of taxa, including Chlorophyta, Phaeo-
phyta and Rhodophyta, from several carbonate-rich
environments throughout the Caribbean and from a
temperate, siliciclastic environment at Woods Hole,
MA, USA. Whereas %C and %N were similar in
macroalgal tissue between these regions (22.6% versus
20.1% and 1.0% versus 1.2%, respectively), P levels
were two-fold lower (0.15% versus 0.07%) in the
carbonate-rich sites of the Caribbean region. We found
parallel results for C. isthmocladum in the present study,
which had similar tissue %N values between southeast
Florida and the Caribbean region, but elevated levels of
%C and depleted levels of %P in the Caribbean region.
The relatively low C:P and N:P ratios of C.
isthmocladum in southeast Florida versus the Caribbean
region indicate P enrichment in southeast Florida
compared to strong P limitation throughout the
Caribbean sites. The strong P limitation in the
Caribbean region may explain the higher %C levels
of C. isthmocladum, which would result from
accumulation of photosynthetic products in the absence
of rapid growth under P limitation. Conversely, reduced
P limitation in the floridian C. isthmocladum popula-
tions suggests that this P enrichment is a primary
physiological factor supporting excessive biomass
development of HABs characterized by rapid growth
and relatively low %C contents. The highest SRP
concentrations in the 1996 nutrient survey in southeast
Florida were near the Boca Raton outfall and off Juno
Beach during a strong upwelling event, suggesting the
importance of P enrichment from both chronic sewage
inputs as well as from natural episodic inputs. More
broadly, the limestone platform of the southeast Florida
study area has been covered with siliciclastic sediments
transported southwards from Piedmont and coastal
plain rivers over geologic time (Meade, 1969; Hine,
1997). This would provide naturally higher background
SRP concentrations compared to those in carbonate-
rich waters of the Caribbean (Lapointe et al., 1992).
Our findings also indicate that strong P limitation
resulting from reduced SRP availability is a major
factor limiting bloom formation of C. isthmocladum in
the Caribbean region. Land-based nutrient discharges
from carbonate-rich islands around the Caribbean
region typically have low SRP concentrations and
high N:P ratios (D’Elia et al., 1981; Lapointe and
Clark, 1992; Lapointe and Thacker, 2002), resulting in
depleted SRP concentrations and strong P limitation in
coastal waters. SRP concentrations in southeast
Florida averaged >0.29 mM during the summer
1996 studies, a value that is an order-of-magnitude
higher than the SRP concentrations reported for
shallow and deep reefs in the Negril Marine Park,
Jamaica, and the Belize Barrier Reef (Lapointe and
Thacker, 2002; Lapointe et al., 1997; Lapointe, 2004).
This regional pattern of depleted SRP in the Caribbean
parallels observations of five-fold higher alkaline
phosphatase activity (APA) in C. isthmocladum at
Discovery Bay, Jamaica, compared to southeast
Florida (Lapointe, 1997), demonstrating the strong
P limitation in Jamaica. The primary P limitation at
Discovery Bay was further evidenced by nutrient
enrichment assays where SRP significantly increased
of the green filamentous alga Chaetomorpha
linum compared to insignificant effects of NO
(Lapointe, 1997). The higher water column SRP
concentrations and reduced P limitation in southeast
B.E. Lapointe et al. / Harmful Algae 4 (2005) 1092–11051100
Florida can support blooms of chlorophyte ‘‘SRP
indicators’’ like C. isthmocladum. This species is
abundant with other SRP indicators (e.g., Ulva,
Chaetomorpha,Enteromorpha) surrounding seabird
rookeries or sewage-impacted waters where elevated
SRP concentrations and low N:P ratios occur
(Lapointe et al., 1993).
The relatively low SRP concentrations on many
carbonate-rich Caribbean reefs would make DOP
cycling an adaptive strategy for macroalgal growth in
these environments. Several phaeophyte genera,
including Dictyota,Sargassum, and Lobophora, have
high capacities for APA and would be favored in
waters with low SRP concentrations. Klausmeier et al.
(2004), using a stoichiometrically explicit model,
suggested that competitive equilibrium favors greater
allocation to biochemical pathways for SRP-poor
resource acquisition (e.g., APA), and therefore, a
higher optimal N:P ratio; exponential growth favors
greater allocation to P-rich assembly processes, and
therefore, a lower N:P ratio. This physiological
mechanism may explain why phaeophytes such as
Dictyota spp. have become dominant bloom species
on reefs formerly dominated by live coral cover in the
nutrient enriched (high N:P) coastal waters of the
Florida Keys (Lapointe and Clark, 1992; Lirman and
Biber, 2000; Lapointe et al., 2004). Similarly, lush
meadows of the phaeophytes Sargassum polyceratium
and Sargassum hystrix, with an extensive understory
of Lobophora variegata (Lapointe, 1997; Lapointe
and Thacker, 2002), have replaced the hermatypic
(reef-forming) coral genera that historically domi-
nated shallow and deep reefs on Jamaica’s north coast
(Goreau, 1959). These Jamaican reefs have also
experienced high N:P ratios associated with human
activities from the upland watershed (D’Elia et al.,
1981; Lapointe, 1997; Lapointe and Thacker, 2002).
Tropical phaeophytes typically have higher %C
content, C:N and C:P ratios than chlorophytes and
rhodophytes (Table 2), indicating their greater ability
for storage of structural C under nutrient limited
growth. This physiological characteristic allows for
the production of C-rich secondary compounds known
to be important for chemical defense from herbivores
in the Phaeophyta. For example, a decrease in
chemical defense production under elevated nitrogen
conditions has been demonstrated in the field for the
temperate Fucus vesiculosus (Yates and Peckol, 1993)
and in laboratory conditions for the tropical Lobo-
phora variegata (Arnold et al., 1995). For phaeo-
phytes, plant phenols tend to accumulate under
environmental conditions where plants have excess
C above the level needed for balanced growth and
where phenylalanine, the substrate of phenylpropa-
noid synthesis, accumulates due to suppressed protein
synthesis (Ilvessalo and Tuomi, 1989). While phaeo-
phytes have not formed widespread HABs on the
northern portion of the Florida Reef Tract (Palm
Beach County), they have formed conspicuous blooms
on reefs in the Florida Keys where considerable
grazing activity occurs (Lapointe and Clark, 1992;
Lirman and Biber, 2000). The extensive meadows of
phaeophytes that have developed on Jamaica’s north
coast have elevated tissue C:N ratios (28; Lapointe
et al., 1992), suggesting that these populations
likewise benefit from the production of anti-herbivore
secondary compounds (e.g., polyphenolics).
4.2. The role of NH
in bloom nutrition in
southeast Florida
The lower N:P ratios of C. isthmocladum in
southeast Florida compared to the Caribbean popula-
tions would not only reduce P limitation, but would also
increase the potential for N limitation on southeast
Florida’s reefs. Enrichment assays with NH
nificantly increased a, the initial slope of the P versus I
curve, of C. isthmocladum compared to insignificant
effects of SRP (Lapointe, 1997). The mean C:N ratio of
C. isthmocladum in southeast Florida (12.2) was lower
than that of Caribbean populations (19.2), suggesting
that the floridian populations were relatively N enriched
relative to C demands. The chronically elevated NH
concentrations reported for this study area (see Fig. 3)
suggest that the availability of NH
would increase
photosynthetic efficiency under low light, leading to
nitrogen saturation of growth and bloomformation (see
Lapointe, 1999).
During summer months, episodic upwelling with
high NO
concentrations occur in the study area
(Atkinson, 1985; Lapointe et al., 2005) and provide
additional enrichment to the NH
and NO
from land-based nutrient inputs. In the Niantic River
estuary, CT, USA, the invasion of C. fragile was
related to NH
enrichment in addition to the available
in that system (Malinowski and Ramus, 1973).
B.E. Lapointe et al. / Harmful Algae 4 (2005) 1092–1105 1101
Nutrient kinetic studies with macroalgae provide
evidence as to why episodic, upwelled NO
, by itself,
could not have historically supported bloom formation
of C. isthmocladum in southeast Florida. In controlled
laboratory studies, Hanisak and Harlin (1978) reported
that uptake of DIN by C. fragile subsp. tomentosoides
was highly dependant upon light, temperature, and the
source of DIN (i.e., NO
versus NH
). At
temperatures of 20–25 8C, the uptake rate of NH
was seven-fold greater than that of NO
and the
presence of NH
inhibited uptake of NO
. Similar
preferences for NH
over NO
have been reported in
other kinetic studies with macroalgae (D’Elia and
DeBoer, 1978) as well as for natural phytoplankton
communities (Conway, 1977). Because an average of
0.82 mMNH
was present in the near-bottom waters
during the summer 1996 upwellings, it is unlikely that
was a major DIN source supporting the C.
isthmocladum blooms. In a seasonal upwelling system
similar to that of southeast Florida, Fujita et al. (1989)
found that relatively low concentrations of NH
(1.22 mM) supplied >100% of the N required for
maximum growth of the chlorophyte Ulva rigida, even
in the presence of much higher NO
(10.8 mM).
4.3. Understanding nutrient enrichment and
eutrophication on coral reefs
Within the past decade, many coral reef biologists
and managers have not fully appreciated the severity
of nutrient enrichment and eutrophication problems
facing coral reefs (Risk, 1999). We suggest that this
has led to the use of inadequate analytical methods and
concomitant misinterpretations of nutrient data. For
example, in the Great Barrier Reef lagoon, the effects
of ‘‘water quality’’ on biomass of Sargassum spp.
transplants from an inshore fringing reef to a mid-shelf
reef (Otter Reef) were assessed (McCook, 1996).
Although no water samples were actually analyzed for
nutrients, McCook (1996) concluded that the ‘‘tissue
analyses indicate that mid-shelf Sargassum transplants
were not limited by nitrogen or phosphorus supplies’’.
However, his reported C:N ratio of 32:1 and C:P ratio
of 1261:1 indicated significant N limitation and severe
P limitation, even higher than that of pelagic
Sargassum in nutrient-depleted surface waters of the
Sargasso Sea (C:P = 877; Lapointe, 1995). McCook’s
study (1996) was cited by Fong et al. (2003) as
evidence that calls into question whether macroalgae
in tropical systems are ever limited by nutrients. Fong
et al. (2003) collected water samples from two sites
on the southwest coast of Puerto Rico. However, their
analytical methods were not sensitive enough
(detection limits of 3.57 mMforNH
and NO
and 1.61 mM for P) to assess nutrient availability in
that oligotrophic environment. Because the resulting
nutrient data of Fong et al. (2003) were below
detection limits, inferences regarding water column
nutrient availability in those studies could not
reasonably be made. Similar problems with inade-
quate detection limits plagued another recent study at
Glover’s Reef offshore the Belize Barrier Reef that
reported background SRP concentrations of 0.36–
1.0 mM(McClanahan et al., 2002). Those values are
some 20-fold higher than the typical SRP concentra-
tions reported for this location (0.05 mM, Lapointe,
2004) and for offshore waters of the Caribbean Sea
(Rajendran et al., 1991). For the coral reefs off
southeast Florida, failure to establish reasonable
background concentrations for NH
have con-
founded the SEFLOE II (Hazen and Sawyer, 1994)
dilution model for the discharge of partially-treated
sewage from ocean outfalls (see Lapointe et al.,
Although macroalgal HABs on coral reefs have
long been attributed to nutrient enrichment and
eutrophication (e.g., Littler, 1973; Banner, 1974;
Johannes, 1975; Smith et al., 1981; Lapointe, 1997),
some reef biologists have concluded that such changes
in benthic community structure on Caribbean coral
reefs result solely from overfishing of herbivorous fish
stocks (Hughes, 1994) and/or loss of keystone grazers,
such as the long-spined sea urchin Diadema antil-
larum (Jackson et al., 2001). However, these conclu-
sions are not supported by numerous grazer reduction
experiments that generally report an expansion of
algal turfs (<2 cm high) rather than macroalgal
blooms (>2 cm high, see Lapointe, 1999)in
oligotrophic environments. These include studies in
the Red Sea (Vine, 1974), Fiji (Littler and Littler,
1997), Belize (Lewis, 1986), the Great Barrier Reef
(Sammarco, 1983), and St. Croix (Carpenter, 1988).
The widely cited study by Lewis (1986) on the Belize
Barrier Reef reported a statistically significant though
relatively small increase (28% over 10 weeks) in algal
B.E. Lapointe et al. / Harmful Algae 4 (2005) 1092–11051102
turfs and no significant increase in the macroalgae
Halimeda sp. and Turbinaria turbinata. These parti-
cular macroalgae have both overgrown coral reefs in the
Negril Marine Park, Jamaica, following decades of
nutrient enrichment from sewage pollution associated
with tourism development and from use of fertilizers for
agriculture (Lapointe and Thacker, 2002). Another
confounding issue is that many invasive, bloom-
forming macroalgae (such as Codium spp.) on reefs
are not preferred by generalist grazers (Ramus, 1971;
Malinowski and Ramus, 1973; Hanisak, 1980; Trow-
bridge, 1995). Overfishing of herbivorous fishes and
other keystone grazers has been implicated as the sole
cause of macroalgal HABs on reefs in southeast Florida
and Jamaica (Hughes et al., 1999) without recognition
of the escalating rate and scale of anthropogenic
nutrient pollution and its consequences to coral reefs
(Lapointe, 1999). This explanation for the decline of
coastal ecosystems (see Jackson et al., 2001), including
the emergence of macroalgal HABs, has been noted and
criticized by Boesch et al. (2001). We encourage coral
reef biologists and managers to consider more broadly
the complex role that escalating nutrient enrichment
plays in the regulation of macroalgal HABs in coral reef
We thank the crew of the R/V Sea Diver for
ensuring safety and for their assistance during our
research cruises in the Caribbean region. For the
Florida research, small boat support was provided by
the Palm Beach County Department of Environmental
Resources Management. The Harbor Branch Envir-
onmental Laboratory (Ft. Pierce, FL, USA) and the
Nutrient Analytical Services Laboratory (University
of Maryland, Solomons, MD, USA) provided analy-
tical support for this work. Two anonymous reviewers
are gratefully acknowledged for improving this
manuscript. This research was supported by the
Florida Sea Grant College Program with support
from NOAA, Office of Sea Grant (Grant #R/C-E-34)
and the National Science Foundation (Grant #DEB-
9400523). This is contribution #1595 from the Harbor
Branch Oceanographic Institution and contribution
#614 from the Smithsonian Marine Station at Fort
Adey, W.H., 1998. Coral reefs: algal structured and mediated
ecosystems in shallow, turbulent, alkaline waters. J. Phycol.
34, 393–406.
Arnold, T.M., Tanner, C.E., Hatch, W.I., 1995. Phenotypic variation
in polyphenolic content of the tropical brown alga Lobophora
variegata as a function of nitrogen availability. Mar. Ecol. Prog.
Ser. 123, 177–183.
Asplia, I., Agemian, H., Chau, A.S.Y., 1976. A semi-automated
method for the determination of inorganic, organic, and total
phosphate in sediments. Analyst 101, 187–197.
Atkinson, L.P., 1985. Hydrography and nutrients of the southeastern
U.S. continental shelf. Oceanogr. Southeast U.S. Cont. Shelf
(AGU) 2, 77–91.
Banner, A.H., 1974. Kaneohe Bay, Hawaii: urban pollution and a
coral reef ecosystem. In: Proceedings of the Second Interna-
tional Coral Reef Symposium, vol. 2. pp. 685–702.
Bell, P.R.F., 1992. Eutrophication and coral reefs: some examples in
the Great Barrier Reef lagoon. Water Res. 26, 553–568.
Bellwood, D.R., Hughes, T.P., Folke, C., Nystoem, M., 2004.
Confronting the coral reef crisis. Nature 429 (6994), 827–
Birkeland, C., 1977. The importance of rate of biomass accumula-
tion in early successional stages of benthic communities to the
survival of coral recruits. In: Proceedings of the Third Inter-
national Coral Reef Symposium, vol. 1. pp. 15–21.
Birkeland, C., 1987. Nutrient availability as a major determinant of
differences among coastal hard-substratum communities in dif-
ferent regions of the tropics. In: Birkeland, C. (Ed.), Comparison
Between Atlantic and Pacific Tropical Marine Coastal Ecosys-
tems: Community Structure, Ecological Processes, and Produc-
tivity. UNESCO Reports in Marine Science 46, pp. 45–97.
Boesch, D.F., Burreson, E., Dennison, W., Houde, E., Kemp, W.,
Kennedy, V., Newell, R., Paynter, K., Orth, R., Ulanowicz, R.,
2001. Factors in the decline of coastal ecosystems. Science 293,
Carlton, J.T., Scanlon, J.A., 1985. Progression and dispersal of an
introduced alga Codium fragile on the Atlantic coast of North
America. Bot. Mar. 28, 155–165.
Carpenter, R.C., 1988. Mass mortality of a Caribbean sea urchin:
immediate effects on community metabolism and other herbi-
vores. Proc. Natl. Acad. Sci. U.S.A. 85, 511–514.
Conway, H.L., 1977. Interaction of inorganic nitrogen in the uptake
and assimilation by marine phytoplankton. Mar. Biol. 39, 221–
D’Elia, C.F., DeBoer, J.A., 1978. Nutritional studies of two red
algae. 2. Kinetics of ammonium and nitrate uptake. J. Phycol.
14, 266–272.
D’Elia, C.F., Webb, K.L., Porter, J.W., 1981. Nitrate-rich ground-
water inputs to Discovery Bay, Jamaica: a significant source of N
to local reefs? Bull. Mar. Sci. 31, 903–912.
D’Elia, C.F., Connor, E.E., Kaumeyer, N.L., Keefe, C.W., Wood,
K.W., Zimmerman, C.F., 1997. Nutrient Analytical Services
Laboratory: Standard Operating Procedures. Technical Report
Series No. 158-97, Chesapeake Biological Laboratory, Solo-
mons, MD, USA.
B.E. Lapointe et al. / Harmful Algae 4 (2005) 1092–1105 1103
Done, T.J., 1992. Phase shifts in coral reef communities and their
ecological significance. Hydrobiology 247 (1), 121–132.
Dubinsky, Z., Stambler, N., 1996. Marine pollution and coral reefs.
Global Change Biol. 2, 511–526.
ECOHAB, 1997. The Ecology and Oceanography of Harmful Algae
Blooms. A National Research Agenda. In: Anderson, D.M.
(Ed.), WHOI, Woods Hole, MA.
Fralick, R.A., Mathieson, A.C., 1973. Ecological studies of Codium
fragile in New England, USA. Mar. Biol. 19, 127–132.
Finkl, C.W., Charlier, R.H., 2003. Sustainability of subtropical
coastal zones in southeastern Florida: challenges for urbanized
coastal environments threatened by development, pollution,
water supply, and storm hazards. J. Coast. Res. 19 (4), 934–
Fong, P., Boyer, K.E., Kamer, K., Boyle, K.A., 2003. Influence of
initial tissue nutrient status of tropical marine algae in response
to nitrogen and phosphorus additions. Mar. Ecol. Prog. Ser. 262,
Fujita, R.M., Wheeler, P.A., Edwards, R.L., 1989. Assessment of
macroalgal nitrogen limitation in a seasonal upwelling region.
Mar. Ecol. Prog. Ser. 53, 293–303.
Goreau, T.F., 1959. The ecology of Jamaican coral reefs. 1. Species
composition and zonation. Ecology 40, 67–90.
Green, C., 1944. Summer upwelling—northeast coast of Florida.
Science 100, 546–547.
Gunsalus, N.M., 1997. High frequency monitoring of wastewater
nutrient discharges and their ecological effects in the Florida
Keys National Marine Sanctuary: Appendix I, Quality Assur-
ance Summary, Nutrient Analysis. Final Report to the Water
Quality Protection Program, United States Environmental Pro-
tection Agency, Marathon, FL.
Hanisak, M.D., 1980. Codium: an invading seaweed. Maritimes 24,
Hanisak, M.D., Blair, S.M., 1988. The deep water macroalgal
community of the East Florida continental shelf (USA). Helgo-
lan. Meeres. 42, 133–163.
Hanisak, M.D., Harlin, M.M., 1978. Uptake of inorganic nitrogen by
Codium fragile subsp. tomentosoides (Chlorophyta) J. Phycol.
14, 450–454.
Hazen and Sawyer, 1994. SEFLOE II Final Report: Broward County
Office of Environmental Services North Regional Wastewater
Treatment Plant; City of Hollywood Utilities Department South-
ern Region Wastewater Treatment Plant; Miami-Dade Water and
Sewer Department North District Wastewater Treatment Plant;
Miami-Dade Water and Sewer Department Central District
Wastewater Treatment Plant Hollywood (FL): Hazen and Saw-
yer. National Oceanic and Atmospheric Administration (AOML,
Miami, FL).
Hine, A.C., 1997. Structural and paleoceanographic evolution of the
margins of the Florida platform. In: Randazzo, F.A., Jones, D.S.
(Eds.), The Geology of Florida. University Press of Florida,
Gainesville, pp. 169–194.
Hughes, T.P., 1994. Catastrophes, phase-shifts, and large-scale
degradation of a Caribbean coral reef. Science 265, 1547–1551.
Hughes, T.P., Szmant, A.M., Steneck, R., Carpenter, R., Miller, S.,
1999. Algal blooms on coral reefs: what are the causes? Limnol.
Oceanogr. 44, 1583–1586.
Ilvessalo, H., Tuomi, J., 1989. Nutrient availability and accumula-
tion of phenolic compounds in the brown alga Fucus vesiculo-
sus. Mar. Biol. 101, 115–119.
Jackson, J.B.C., et al., 2001. Historical over-fishing and the recent
collapse of coastal ecosystems. Science 293, 629–638.
Johannes, R.E., 1975. Pollution and degradation of coral reef
communities. In: Wood, E., Johannes, R.E. (Eds.), Tropical
Marine Pollution. Elsevier, New York, pp. 13–51.
Klausmeier, C.A., Lichtman, E., Daufresne, T., Levin, S.A., 2004.
Optimal nitrogen-to-phosphorus stoichiometry of phytoplank-
ton. Nature 429, 171–174.
Lapointe, B.E., 1987. Phosphorus and nitrogen-limited photosynth-
esis and growth of Gracilaria tikvahiae (Rhodophyceae) in the
Florida Keys: an experimental field study. Mar. Biol. 93, 561–
Lapointe, B.E., 1995. A comparison of nutrient-limited productivity
in Sargassum natans from neritic vs. oceanic waters of the
western North Atlantic ocean. Limnol. Oceanogr. 40 (3),
Lapointe, B.E., 1997. Nutrient thresholds for bottom-up control of
macroalgal blooms on coral reefs in Jamaica and southeast
Florida. Limnol. Oceanogr. 42 (5, part 2), 1119–1131.
Lapointe, B.E., 1999. Simultaneous top-down and bottom-up forces
control macroalgal blooms on coral reefs (reply to the comment
by Hughes et al.) Limnol. Oceanogr. 44 (6), 1586–1592.
Lapointe, B.E., 2004. Phosphorus-rich waters at Glovers Reef
Belize? Mar. Poll. Bull. 48, 193–195.
Lapointe, B.E., Clark, M., 1992. Nutrient inputs from the watershed
and coastal eutrophication in the Florida Keys. Estuaries 15,
Lapointe, B.E., Hanisak, M.D., 1997. Algal blooms in coastal
waters: eutrophication on coral reefs of southeast Florida. Final
Report, Florida Sea Grant Project R/C-E-34.
Lapointe, B.E., Thacker, K., 2002. Community-based water quality
and coral reef monitoring in the Negril Marine Park, Jamaica:
land-based nutrient inputs and their ecological consequences. In:
Porter, J.W., Porter, K.G. (Eds.), The Everglades, Florida Bay,
and Coral Reefs of the Florida Keys: An Ecosystem Sourcebook.
CRC Press, Boca Raton, FL, pp. 939–963.
Lapointe, B.E., Littler, M.M., Littler, D.S., 1992. Nutrient avail-
ability to marine macroalgae in siliciclastic versus carbonate-
rich coastal waters. Estuaries 15, 75–82.
Lapointe, B.E., Littler, M.M., Littler, D.S., 1993. Modification of
benthic community structure by natural eutrophication: the
Belize Barrier reef. In: Proceedings of the Seventh International
Coral Reef Symposium, vol. 1. pp. 323–333.
Lapointe, B.E., Littler, M.M., Littler, D.S., 1997. Macroalgal over-
growth of fringing coral reefs at Discovery Bay, Jamaica:
Bottom-up versus top-down control. In: Proceedings of the
Eighth International Coral Reef Symposium, vol. 1. pp. 927–
Lapointe, B.E., Barile, P.J., Matzie, W.R., 2004. Anthropogenic
nutrient enrichment of seagrass and coral reef communities in
the Lower Florida Keys: discrimination of local versus regional
nitrogen sources. J. Exp. Mar. Biol. Ecol. 308 (1), 23–58.
Lapointe, B.E., Barile, P.J., Littler, M.M., Littler, D.S., 2005.
Macroalgal blooms on southeast Florida coral reefs. II. Cross-
B.E. Lapointe et al. / Harmful Algae 4 (2005) 1092–11051104
shelf discrimination of nitrogen sources indicates widespread
assimilation of sewage nitrogen. Harmful Algae 4, 1106–1122.
Larned, S.T., Stimson, J., 1996. Nitrogen-limited growth in the coral
reef chlorophyte Dictyosphaeria cavernosa, and the effect of
exposure to sediment-derived nitrogen on growth. Mar. Ecol.
Prog. Ser. 145, 95–108.
Lewis, S., 1986. The role of herbivorous fishes in the organization of
a Caribbean reef community. Ecol. Monogr. 56, 183–200.
Lirman, D., Biber, P., 2000. Seasonal dynamics of macroalgal
communities of the northern Florida Reef Tract. Bot. Mar.
43, 305–314.
Littler, M.M., 1973. The population and community structure of
Hawaiian fringing-reef crustose corallinaceae (Rhodophyceae,
Cryptonemiales). J. Exp. Mar. Biol. Ecol. 11, 103–119.
Littler, D.S., Littler, M.M., 2000. Caribbean Reef Plants. Offshore
Graphics, Washington, DC.
Littler, M.M., Littler, D.S., Lapointe, B.E., 1993. Modification of
tropical reef community structure due to cultural eutrophication:
the southwest coast of Martinique. In: Proceedings of the
Seventh International Coral Reef Symposium, vol. 1. pp.
Littler, M.M., Littler, D.S., 1997. Disease-inducedmass mortality of
crustose coralline algae on coral reefs provides rationale for the
conservation of herbivorous fish stocks. In: Proceedings of the
Eighth International Coral Reef Symposium, vol. 1, pp. 719–
Malinowski, K.C., Ramus, J., 1973. Growth of the green alga
Codium fragile in a Connecticut estuary. J. Phycol. 9, 102–110.
Meade, R.H., 1969. Landward transport of bottom sediments in the
estuaries of the coastal plain. J. Sediment. Petrol. 39, 229–234.
McClanahan, T.R., Cokos, B.A., Sala, E., 2002. Algal growth and
species composition under experimental control of herbivory,
phosphorus and coral abundance in Glovers Reef, Belize. Mar.
Poll. Bull. 44, 441–451.
McConnaughey, T.A., Adey, W.H., Small, A.M., 2000. Community
and environmental influences on reef coral calcification. Limnol.
Oceanogr. 45 (7), 1667–1671.
McCook, L.J., 1996. Effects of herbivores and water quality on
Sargassum distribution on the central Great Barrier Reef: cross-
shelf transplants. Mar. Ecol. Prog. Ser. 139, 179–192.
National Research Council, 1995. Understanding Marine Biodiver-
sity. Ocean Studies Board, Biology Board.
National Research Council, 2000. Clean Coastal Waters: Under-
standing and Reducing the Effects of Nutrient Pollution. Ocean
Studies Board, Water Science and Technology Board.
Rajendran, M., Kumar, D., Kahan, A.D., Knight, D., O’Reilly, A.,
Yen, I.C., Wagh, A.B., Desai, B.N., 1991. Some aspects of
nutrient chemistry of the Caribbean Sea. Caribb. Mar. Stud. 2
(1 and 2), 81–86.
Ramus, J., 1971. Codium: the invader. Discovery 6, 59–68.
Risk, M.J., 1999. Paradise lost: how science and management failed
the world’s coral reefs. Mar. Freshwater Res. 50, 831–837.
Sammarco, P.W., 1980. Diadema and its relationship to coral spat
mortality: grazing, competition, and biological disturbance. J.
Exp. Mar. Biol. Ecol. 45 (2–3), 245–272.
Sammarco, P.W., 1982. Effects of grazing by Diadema antillarum
Philippi (Echinodermata: Echinoidea) on algal diversity and
community structure. J. Exp. Mar. Biol. Ecol. 65 (1), 83–105.
Sammarco, P.W., 1983. Effects of fish grazing and damselfish
territoriality on coral reef algae. I. Algal community structure.
Mar. Ecol. Prog. Ser. 13, 1–14.
Schaffelke, B., Klumpp, D.W., 1998. Nutrient-limited growth of the
coral reef macroalga Sargassum baccularia and experimental
growth enhancement by nutrient addition in continuous flow
culture. Mar. Ecol. Prog. Ser. 164, 199–211.
Silva, P.C., 1957. Codium in Scandinavian waters. Stensk Botanisk
Tidskrift 51, 117–134.
Smith, S.V., Kimmerer, W.J., Laws, E.A., Brock, R.E., Walsh, T.W.,
1981. Kaneohe Bay sewage diversion experiment: perspectives
on ecosystem response to nutritional perturbation. Pac. Sci. 35,
Taylor, C., Stewart, H., 1958. Summer upwelling along the east
coast of Florida. J. Geophys. Res. 64, 33–39.
Tomascik, T., Sander, F., 1987. Effects of eutrophication on reef
building corals. II. Structure of scleractinian coral communities
on fringing reefs, Barbados, West Indies. Mar. Biol. 94, 53–75.
Trowbridge, C.D., 1995. Establishment of the green alga Codium
fragile ssp. on New Zealand rocky shores: current distribution
and invertebrate grazers. Ecology 83, 949–965.
Trowbridge, C.D., 1998. Ecology of the green macroalga Codium
fragile: invasive and non-invasive subspecies. Ann. Rev. Ocea-
nogr. Mar. Biol. 36, 1–64.
UNEP, 1994. Regional overview of land-based sources of pollution
in the wider Caribbean region. Caribbean Environment Program
Technical Report 33, UNEP Caribbean Environment Program,
Kingston, Jamaica.
Urnezis, C.M., 1995. Alkaline phosphatase activity and phosphorus
limitation in marine macroalgae from the Florida Keys and the
Bahamas. Master’s Thesis. Nova Southeastern University, Ft.
Lauderdale, FL.
USEPA, 2003. Relative risk assessment of management options for
treated wastewater in south Florida. Office of Water. EPA 816-R-
Vine, P.J., 1974. Effects of algal grazing and aggressive behaviour of
the fishes Pomacentrus lividus and Acanthurus sohal on coral-
reef ecology. Mar. Biol. 24 (2), 131–136.
Yates, J.L., Peckol, P., 1993. Effects of nutrient availability and
herbivory on polyphenolics in the seaweed Fucus vesiculosis.
Ecology 74, 1757–1766.
B.E. Lapointe et al. / Harmful Algae 4 (2005) 1092–1105 1105
... Previous studies showed that species diversity and taxonomic composition of the main groups of algae differ between pollution-free regions and those exposed to nutrient pollution [1][2][3][4]. Our monitoring studies (2008)(2009)(2010)(2011)(2012)(2013)(2014)(2015)(2016)(2017) have shown that Sanya Bay is contaminated with nutrients discharged from the local urban sewage system and aquaculture farms. ...
... As shown by previous studies in various regions of the World Ocean [3,4,7,10,12,[14][15][16][17], high concentrations of nutrients in seawater induce algal blooms: the biomass of algae (especially green and brown ones) increases multifold and their diversity decreases. Our previous and current studies do not contradict this observation [7]. ...
... All of the above findings indicate that the coral reef located opposite the wastewater outlet from the fish farm and exposed to heavy pollution from the farm is degrading and shifting into a "plant reef". A similar phenomenon was first reported from the Gulf of Mexico, where the degradation of a reef was caused by high eutrophication due to mineral fertilizers discharged with surface runoff from agricultural fields [3,4]. ...
... Many stable isotope studies using POM or nitrate δ 15 N values have previously focused either on: (1) characterizing end-member inputs and progressive mixing within watersheds and their estuaries (e.g., McClelland et al., 1997); (2) quantifying non-conservative transformations of N species during passage through riverine and estuarine waters (e.g., Cifuentes et al., 1989;Mariotti et al., 1984;Middleburg and Nieuwenhuize, 2000); or (3) identifying temporal and/or spatial gradients in nearshore marine waters by analyzing producer or consumer δ 15 N values (e.g., Sammarco et al., 1999;Umezawa et al., 2002;Lapointe et al., 2005). In one of the first studies to use an integrated approach to link nitrogen in estuarine producers with anthropogenic sources of wastewater inputs, McClelland and Valiela (1998) observed that producer δ 15 N increased in a 1:1 manner as groundwater nitrate δ 15 N values increased with the 15 N-enriched wastewater contributions to the total N pool. ...
We use a multi-tracer approach to identify catchment sources of nitrogen (N) in the skeletons of nearshore Porites corals within the Great Barrier Reef. We measured δ¹⁵N, δ¹³C and C:N ratios of particulate organic matter (POM) sampled from the Pioneer River catchment and identified five distinct end-members: (1) marine planktonic and algal-dominated matter with higher δ¹⁵N values from the river mouth and coastal waters; (2) estuarine planktonic and algal matter with lower δ¹⁵N values associated with estuarine mixing; (3) lower river freshwater phytoplankton and algal-dominated matter in stratified reservoirs adjacent to catchment weirs, with the ¹⁵N-enriched source likely caused by microbial remineralization and denitrification; (4) upper river low δ¹⁵N terrigenous soil matter eroded from cane fields bordering waterways; and (5) terrestrial plant detrital matter in forest streams, representing a low δ¹⁵N fixed atmospheric nitrogen source. The δ¹⁵N values of adjacent, nearshore Porites coral skeletons is reflective of POM composition in coastal waters, with ¹⁵N-enriched values reflective of transformed N during flood pulses from the Pioneer River.
... Along the PCO1 and PCO2, the higher concentration of NH 4 + evidenced the eutrophication at PAM, Co, Pu, DS, C70, and BSA sites (see Fig. 4 and Table 2) and in most reefs of this littoral (except Sa and Ca) due to sewage input over the 2008-2016 period. Sewage discharge has increased NH 4 + levels in other Caribbean reefs and Florida Keys (Lapointe et al. 2004(Lapointe et al. , 2005(Lapointe et al. , 2011, and only at Sa and Ca reefs between 0.2 and 0.5 μmol/L, characteristic of reefs with low nutrient levels (Furnas 1991). In this way, the positive association between δ 15 N of E. flexuosa and P. kuekenthali and concentration of NH 4 + (see Figs. 3 and 4) showed that the higher δ 15 N in both species and the higher NH 4 + levels are due to continuous sewage discharge coming from the polluted watersheds to the coastline of Havana City. ...
Full-text available
Eutrophication is one of the causes of the degradation of reefs worldwide. The aim of this research is to determine if sewage discharge reaches the fore reefs at northwest of Cuba using δ15N in tissues of the octocorals Eunicea flexuosa and Plexaura kuekenthali and the concentration of microbiological and physical-chemical variables. Thirteen reefs at 10-m depth were selected near river basins and far from the urban and industrial development of Havana City. Branch tips of both species were collected, the concentrations of nutrient and microorganisms in water samples were quantified, and horizontal visibility in the water (Vis) was determined. Overall, δ15N of E. flexuosa ranged from 1.5 to 6.3‰ and P. kuekenthali from 1.7 to 6.7‰. The tissue of both species was significantly enriched in 15N in reefs near polluted watersheds compared with reefs far from pollution by anthropogenic activities. The δ15N of both species showed a positive and significant correlation with the concentration of fecal and total coliform bacteria, heterotrophic bacteria, and NH4+ and a negative and significant correlation with the Vis. The δ15N of the two species and microbiological and physical-chemical variables evidenced water quality decline by sewage discharge that reached reefs near polluted watersheds.
... It has been shown that Sanya Bay is 2-2.5 times more polluted than Haitang Bay. Previous studies have reported that floristic ratios of the major algal groups are changed between clean and nutrient-polluted regions [23][24][25][26]. High concentrations of DIN and orthophosphates promote species diversity, high photosynthetic rate and biomass accumulation of the filamentous green algae, and also frondose brown algae of families such as the Sargassaceae and Dictyotaceae [17]. ...
... Tourism Advertising Revolving Fund and 85% to the Territory's General Fund (The Virgin Islands Revenue Enhancement and Economic Recovery Act of 2017). Increased coastal nutrient input and pollution Improvements to wastewater management and infrastructure [90,91] Approximately half of the sewer lines in the U.S. are past the midpoint of their life cycle (U.S. EPA, 2002). President Trump proposed infrastructure plans that included financing for major water infrastructure development (The White House 2018, 2020). ...
As many as 1 billion people across the planet depend on coral reefs for food, coastal protection, cultural practices, and income [1, 2]. Corals, the animals that create these immensely biodiverse habitats, are particularly vulnerable to climate change and inadequately protected. Increasing ocean temperatures leave corals starved as they lose their primary source of food: the photosynthetic algae that live within their tissue. Ocean warming has been impacting coral reefs around the globe for decades, with the latest 2014-2016 heat stress event affecting more than 75% of the world’s corals [3, 4]. Here, we discuss the benefits humans derive from healthy reefs, the threats corals face, and review current policies and management efforts. We also identify management and policy gaps in preserving coral habitats. The gain and urgency of protecting coral reefs is evident from their vast economic and ecological value. Management and restoration efforts are growing across the globe, and many of these have been influential in mitigating local stressors to reefs such as overfishing, nutrient inputs, and water quality. However, the current trajectory of ocean temperatures requires sweeping global efforts to reduce greenhouse gas emissions in order to effectively safeguard the future of coral reefs. The U.S. should stand as a world leader in addressing climate change and in preserving one of the planet’s most valuable ecosystems.
Most tropical estuarine and coastal environments are impacted by humankind; only some remote habitats are pristine. There is increasing recognition that coastal pollution problems are linked to contamination of adjacent watersheds and catchments, and aerosols in the lower atmosphere. Heavy metals, nutrients, petroleum hydrocarbons, plastics and other debris, and organic wastes such as pesticides, herbicides, and organochlorine chemicals are all types of industrial and agricultural waste that wash into streams and rivers and ultimately down into estuaries and the adjacent coastal zone. Metals come from the earth's crust, found in rocks, soils and sediments, but they can become contaminants when they are concentrated by industrial activity. Tropical sandy beaches and sand and mud flats, especially in Brazil and India, are subject to eutrophication to the extent that beaches must often be closed due to high faecal coliform counts.
Full-text available
Tropical coastal waters are highly dynamic and amongst the most biogeochemically active zones in the ocean. This review compares nitrogen (N) and phosphorus (P) cycles in temperate and tropical coastal waters. We review the literature to identify major similarities and differences between these two regions, specifically with regards to the impact of environmental factors (temperature, sunlight), riverine inputs, groundwater, lateral fluxes, atmospheric deposition, nitrogen fixation, organic nutrient cycling, primary production, respiration, sedimentary burial, denitrification and anammox. Overall, there are some similarities but also key differences in nutrient cycling, with differences relating mainly to temperature, sunlight, and precipitation amounts and patterns. We conclude that due to the differences in biogeochemical processes, we cannot directly apply cause and effect relationships and models from temperate systems in tropical coastal waters. Our review also highlights the considerable gaps in knowledge of the biogeochemical processes of tropical coastal waters compared with temperate systems. Given the ecological and societal importance of tropical coastal waters, we hope that highlighting the differences and similarities to temperate systems as well as the existing gaps, will inspire further studies on their biogeochemical processes. Such knowledge will be essential to better understand and forecast impacts on tropical coastal nutrient cycling at local, regional, and global scales.
Full-text available
Tropical coral reefs are hotspots of biodiversity, provide important ecosystem services and belong to the most productive ecosystems on earth, although they flourish in oligotrophic, i.e., nutrient-poor waters where nitrogen (N) is scarce. As such, efficient uptake, recycling and removal mechanisms of N by coral reef organisms and substrates, including the key reef ecosystem engineers, the hard corals, are of paramount importance. However, a holistic understanding of microbially performed N cycling is still missing. Previous studies have demonstrated that microbes capable of fixing atmospheric dinitrogen (N2; diazotrophs) provide bioavailable N to the coral reef organisms. Hypothesised counteracting N-removing mechanisms like denitrification, hence, may help to maintain low N conditions, and ultimately coral (reef) functioning. Hence, N availability in coral reef environments is partly a consequence of the interplay between N2 fixation and denitrification, but knowledge particularly on denitrification is missing. As coral reefs and their functioning are adapted to oligotrophic environments, environmental alterations such as eutrophication could potentially evoke ecosystem responses, and subsequently, directly affect biogeochemical pathways. The present thesis aims to extend current knowledge on biogeochemical cycling of N in coral reefs by targeting the following research goals: i) developing a new method to simultaneously determine N2 fixation and denitrification and quantifying N fluxes in and ex situ; ii) assessing baseline rates of N2 fixation and denitrification for major functional groups and assessing their relative importance in intact coral- and degraded algae-dominated reef communities; and iii) investigating the effects of short- and long-term eutrophication on both aforementioned N cycling pathways. Hypothetically, similar to N2 fixation, denitrification is an active microbially performed N cycling pathway in coral reef organisms and substrates, with eutrophication evoking suppressing and stimulating responses, respectively, of N2 fixation and denitrification activity. The experimental work consisted of a combination of physiological and molecular tools and was carried out in situ and ex situ at the central Red Sea. Methods established during the present dissertation allow the simultaneous quantification of N2 fixation and denitrification by combining commonly applied acetylene-based incubation methods. Further, community-wide N fluxes were also quantified in situ using benthic incubation chambers. Findings of the present thesis reveal that denitrification, like N2 fixation, is an active pathway in all investigated coral reef substrates and organisms. On an ecosystem level, important N2 fixers such as turf algae and coral rubble exhibit ~100-fold higher N2 fixation rates compared to corals, but these substrates are less involved in processing nitrogenous compounds via denitrification. On the other hand, soft corals show 2- to 4-fold higher denitrification rates than turf algae or coral rubble and can thus be characterised as key denitrifiers in reef environments. Extrapolated to coral- and algae-dominated reef areas, turf algae and coral rubble contribute to > 90 % of fixed N in both reef areas, whereas > 50 % of total denitrification was performed by corals in degraded reef areas. In situ long-term (8 weeks) eutrophication experiment stimulated both N2 fixation and denitrification in turf algae, a hard coral and reef sands. Further, a substrate-specific and nutrient concentration-dependant threshold that modulates N2 fixation and denitrification in coral rubble was observed, as rapid responses in N cycling activities were observed. In conclusion, using the newly established methods during the thesis, denitrification was identified as an actively performed pathway in coral reef environments. Interestingly and against hypothesis, the effects of eutrophication on N cycling pathways are divergent, with both suppressing and stimulating effects on N2 fixation and denitrification. Altogether, higher N availability in algae-dominated reefs through high amounts of N2 fixation may facilitate higher growth rates of reef algae, ultimately resulting in a positive feedback loop (on the budget of bioavailable N), particularly under moderately and realistic nutrient-enriched scenarios. In contrast, coral rubble may inhibit a key role under very eutrophic conditions, as an N-dependant threshold was identified that stimulates denitrification and suppresses N2 fixation. As such, coral rubble might alleviate excess N from coral reefs via processing N via denitrification. In how far divergent responses of N2 fixation and denitrification to eutrophication might be further suppressed, counteracted or stimulated due to further anthropogenic stressors such as ocean warming remains to be targeted in future studies. Based on the findings here, future management efforts should ultimately focus on the prevention of local N eutrophication.
Full-text available
Nitrogen (N) is a limiting nutrient in highly productive tropical coral reefs, despite its key role for primary production. This requires efficient (re)cycling of N by the dwelling organisms, including the key reef ecosystem engineers, the hard corals. As such, corals evolved symbiotic relationships with eukaryotic and prokaryotic microbes, together called a holobiont, which aid in nutrient acquisition and recycling. The nutrient exchange symbiosis between the coral host and the eukaryotic photosynthetic dinoflagellates of the family Symbiodiniaceae has given corals an ecological advantage over other functional groups such as algae. The Symbiodiniaceae provide the coral host with carbon (C) rich photosynthates, while in return, the Symbiodiniaceae receive N and phosphorus (P). Additionally, diazotrophs, microbes capable of fixing atmospheric dinitrogen (N2), can provide the coral holobiont with bioavailable N. Coral holobionts benefit from low internal availability of N as N-limitation may maintain steady translocation of the photosynthates on which the corals rely. Thus, coral holobionts may be particularly susceptible to increases in (environmental) dissolved inorganic N (DIN) due to e.g. anthropogenic input, or stimulated activity of diazotrophs. As such, corals likely have mechanisms in place for the alleviation of excess N, i.e. denitrification, which may ultimately aid coral functioning. This thesis aims at extending the current knowledge on biogeochemical cycling of N associated with coral holobionts. Specifically, in addition to N2 fixation, we tested whether the antagonistic N-cycling pathway to N2 fixation, i.e. denitrification, is an active pathway in coral holobionts and whether it is affected by environmental change. In addition, we measured N-cycling pathways associated with other coral reef organisms and substrates under environmental change. This allowed us to make inferences for coral reef functioning when exposed to global and local stressors. We applied a combination of physiological and molecular analyses and used the strong seasonality of the northern and central Red Sea as a natural laboratory. Our findings reveal that denitrification was actively associated with all investigated coral species. Similar to diazotrophy, denitrification may thus be ubiquitously associated with coral holobionts. Under stable environmental conditions, denitrification and N2 fixation aligned and both N-cycling pathways correlated with Symbiodiniaceae cell densities. Thus, the relationship between denitrification and N2 fixation may be the result of a shared organic C limitation (by translocated photosynthates from the Symbiodiniaceae) within the holobiont. Higher seasonal availability of DIN (leading to higher DIN:dissolved inorganic P [DIP] ratios) dynamically shifted the ratio of denitrifiers and diazotrophs, in favour of the denitrifiers. The proliferation of Symbiodiniaceae suggests incomplete alleviation of excess N by denitrification. Indeed, Symbiodiniaceae cell densities also correlated with environmental DIN availability. In response to moderate in situ eutrophication of DIN and DIP, both N-cycling pathways more than doubled in activity. Surprisingly, the Symbiodiniaceae populations remained stable. In addition, there was no significant incorporation of N originating from the eutrophication event in the Symbiodiniaceae. This suggests that N-limitation was maintained, likely assisted by denitrification. These findings suggest that the dynamic interplay of denitrification and N2 fixation may regulate Symbiodiniaceae populations, but the extent to which they maintain N-limitation may depend on the environmental availability of DIN and DIP. By comparing coral holobiont associated N-cycling to other functional groups on coral reefs, we postulate that under local and global stress scenarios, coral holobionts may lose the competition for space to algae as they 1) can strongly capitalize on (anthropogenic) nutrient inputs, 2) have high associated N2 fixation VI rates that increase in response to ocean warming and moderate N/P eutrophication, and/or 3) have low associated denitrification. Turf algae and coral rubble exhibited ∼100-fold higher N2 fixation rates compared to hard corals. Contrastingly, denitrification rates were as low as those associated with hard corals. Therefore, coral reefs in the process of shifting towards algae dominance may get caught in a positive feedback loop where dead coral (coral rubble) is rapidly overgrown by algae which in return naturally provide the reef with bioavailable N. This may facilitate higher growth rates of reef algae. Collectively, the results described in this thesis suggest that the interplay of N2 fixation and denitrification associated with coral holobionts may indeed aid in coral functioning by maintaining healthy populations of Symbiodiniaceae. Increased activity of diazotrophs induced by thermal stress, both associated with the coral holobiont and other dwelling organisms, as well as eutrophication of N may ultimately shift the coral holobionts’ internal N:P ratios towards P limitation as denitrifiers may be unable to alleviate excess N. Thus, future management efforts should focus strongly on the local prevention of N eutrophication and the mitigation of global warming.
The subtropical Atlantic coastal zone of southeastern Florida supports nearly 7 million inhabitants on a coastal plain conurbation that stretches from West Palm Beach to Miami. About a quarter of the present population originally settled on higher topography along the shore-parallel Atlantic Coastal Ridge. From about the middle 1900s, however, urbanization intensified along the shore and spread westward into freshwater marshlands. Population densities approaching 2500 persons per km-2 along some coastal sectors and dredge and fill operations to create urban land in western marshes degraded coastal environments bringing in question sustainability. Efforts to maintain environmental integrity initially focused on shore protection first via "hard" engineering works, which later ont included massive beach renourishment projects along developed coasts subject to critical erosion. Marine algal blooms, led to eutrophication, degraded coastal water quality, and deterioration of coral reefs indicate environmental problems at least as serious as beach erosion. Recognition of a potential eco-catastrophe, collapse of entire marine and coastal wetland ecosystems in southern Florida, led turn to the Everglades Restoration Project, the largest single environmental recovery effort in the world. Cleanup of terrestrial systems is essential to sustainability of marine ecosystems now jeopardized by nutrient loading. Serious degradation of the Florida Reef Tract, a coral-algal barrier reef system, is beyond question as extensive sectors of coral reef die from increased loading of nearshore waters by elevated nitrogen (N) and phosphorus (P) nutrient levels delivered to the coast by submarine groundwater discharge (SGD). The source of N-P input into the Biscayne Aquifer, which has one of the highest carbonate aquifer transmissivities in the world, is sugar cane farming in the Everglades Agricultural Area on the inner portion of the coastal plain. Groundwater discharges for Palm Beach County are, for example, estimated from a groundwater MODFLOW model at 1,659 X 106 m3 yr -1. Total N in groundwater below the coastal plain adjacent to remnant Everglades averages about 1.25 mg l-1. SGD nutrient fluxes to the coast are 5727 and 414 metric tons per year for P and N, respectively. Surface water contributions for P and N are respectively 197 and 2,471 metric tons per year. Nutrient delivery to beach and nearshore environments is a serious problem that threatens coastal water quality which in turn will impact tourism-related activities such as sunbathing, beach walking, swimming, snorkeling, SCUBA diving, and surf fishing. The full magnitude of the problem has yet to surface because it takes about three to eight decades for groundwater from the interior parts of the coastal plain to reach the nearshore zone. Pollution of groundwater increases with time due to higher doses of fertilizers on croplands and runoff from expanding urban areas. Solutions to present environmental threats are obvious and, perhaps surprisingly, do not fall within the scientific arena because causes and remedies are already known and future impacts are anticipated. The present environmental cleanup efforts, which are of mammoth proportions and financial cost, are doomed to failure until the causes of problems are eliminated or neutralized. Even though sustainable management procedures are well known, sustainability cannot be achieved by treating symptoms. Sustainable coastal habitats in subtropical southeast Florida will be secured when there is application of best management practices based on environmental ethics rather than capital gain, development of political will directed towards continuous multiple land use rather than terminal single use, and inculcation of pro-active public perception of best land management practices rather than politically-correct land-use policies.