Land-Based Nutrient Enrichment of the Buccoo Reef Complex and
Fringing Coral Reefs of Tobago, West Indies
Brian E. Lapointe1*, Richard Langton2, Bradley J. Bedford1, Arthur C. Potts3, Owen Day2, and
Chuanmin Hu4
1
Center for Marine Ecosystem Health, Harbor Branch Oceanographic Institute at Florida
Atlantic University, 5600 US Highway One, Fort Pierce, FL, 34946 U.S.A.
2
Buccoo Reef Trust, Cowie’s Building, Auchenskeoch Road, Carnbee Junction, Carnbee,
Tobago, W. I.
3
University of Trinidad and Tobago, c/o Centre for Marine Sciences, Institute of Marine Affairs,
Hill Top Lane, Chaguaramas, P.O. Box 3160, Carenage, Trinidad and Tobago, W.I.
4
College of Marine Science, University of South Florida, St. Petersburg, FL 33701 U.S.A.
*Corresponding author; Tel.: 772-465-2400 ext 276; fax: 772-468-0757
e-mail address: blapoin1@hboi.fau.edu
Key words: coral reef, macroalgae, eutrophication, sewage, nitrogen, phosphorus, Orinoco River,
Tobago, nutrient pollution, remote sensing
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Abstract
Tobago’s fringing coral reefs (FR) and Buccoo Reef Complex (BRC) can be affected locally, by
wastewater and stormwater, and regionally by the Orinoco River. In 2001, seasonal effects of
these inputs on water column nutrients and phytoplankton (Chl a), macroalgal C:N:P and 15N
values, and biocover at FR and BRC sites were examined. Dissolved Inorganic Nitrogen (DIN,
particularly ammonium) increased while soluble reactive phosphorus (SRP) decreased from the
dry to wet season. Wet season satellite and Chl a data showed that Orinoco runoff reaching
Tobago contained chromophoric dissolved organic matter (CDOM) but little Chl a, suggesting
minimal riverine nutrient transport to Tobago. C:N ratios were lower (16 vs 21) and macroalgal
15N values higher (6.6 vs 5.5 ‰) in the BRC versus FR, indicating relatively more wastewater
N in the BRC. High macroalgae and low coral cover in the BRC further indicate that better
wastewater treatment could improve the health of Tobago’s coral reefs.
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1. Introduction
Coral reefs are biologically diverse, economically valuable ecosystems that provide an
array of ecological services to coastal communities. Coral reefs flourish in tropical and
subtropical oligotrophic waters and are susceptible to eutrophication as a result of low level
nutrient pollution (Johannes, 1975; NRC, 2000). Early studies in Kaneohe Bay, Hawaii, showed
that reef corals can be overgrown by macroalgae when small increases in nutrient concentrations
(nitrogen and/or phosphorus) occur as a result of sewage pollution (Banner, 1974; Smith et al.,
1981). In the Caribbean region, pollution from land-based sources is considered one of the most
important threats to the marine environment and to the sustainable use of its resources (UNEP,
1994). Sources of nutrient pollution include sewage outfalls, septic tanks, stormwater runoff,
fertilizers, deforestation (Likens, 2001; Andréfouët et al., 2002; Hu et al., 2003&2004a; Lapointe
and Thacker, 2002; ), and atmospheric deposition (Barile and Lapointe, 2005; Paerl et al., 2002).
The Republic of Trinidad & Tobago is located at the southern end of the Lesser Antilles
off the coast of Venezuela and is affected seasonally by discharges from the Orinoco River
(Laydoo, 1991). Tobago is less influenced by the Orinoco River than Trinidad, which accounts
for considerable coral reef growth over the volcanic substrata of Tobago, especially in the
southwestern area where extensive reef development has resulted in a shallow limestone
platform known as the Buccoo Reef Complex (BRC; Fig. 1). The BRC encompasses an area of
~ 7 km2 and was officially designated a marine protected area, Buccoo Reef Marine Park
(BRMP), in 1973 (Laydoo, 1991). The BRMP is the best example of a contiguous mangroveseagrass-coral reef ecosystem in Trinidad & Tobago and is a major economic asset, attracting
tens of thousands of visitors per year.
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Like most marine protected areas in the Caribbean region, creation of the BRMP has not
protected the area from water quality degradation. Many coastal dwellings in the adjacent
Buccoo Village area, for example, have septic tanks and “soak-away” systems dug into the
porous limestone which overlies the island’s volcanic foundation. This rudimentary sewage
disposal technology provides little removal of nitrogen, which is highly mobile in carbonate-rich
systems and is transported via groundwater into coastal waters (Lapointe et al., 1990; Costa et
al., 2000; Lapointe and Thacker, 2002). Similarly, secondarily treated sewage, a technology that
does not remove dissolved nutrients sufficiently to protect coral reef ecosystems, enters Buccoo
Bay and the Bon Accord Lagoon from several sewage treatment plants servicing subdivisions
near Buccoo Village (Coral Garden Estates) and Bon Accord. Sewage pollution in Buccoo Bay
presents a significant risk to public health as indicated by chronically elevated coliform bacteria
and fecal streptococci counts (John, 1996).
There has long been concern about sewage pollution in the BRC, but little study of how it
drives the eutrophication and degradation of these coral reef communities. Kenny (1976)
provided one of the first qualitative studies of coral communities in the BRC and noted that “care
should be taken not to increase run-off from the adjacent land and to restrict the entry of
pollutants.” Laydoo and Heileman (1987) sampled effluents from sewage treatment plants
servicing subdivisions on the watershed of the BRC and recommended upgrading the treatment
facilities throughout the Buccoo Reef watershed. In 1994, the Institute of Marine Affairs
completed a management plan for the BRMP (IMA, 1994) that specifically recognized sewage
impacts (i.e. fecal coliform contamination) in the inshore waters of Buccoo Bay, but the plan did
not address the chronic ecological impacts of nutrient pollution on the coral reef communities.
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Like the BRC, other fringing reefs around Tobago’s coast could be receiving increasing
nutrient loads from inadequately treated sewage effluent. Both large and small communities rely
on “soak-aways”, as on the BRC watershed, or on centralized sewage collection and treatment
systems that provide, at best, secondary treatment (no nutrient removal) and are usually
undersized, resulting in nutrient-rich effluent discharges into rivers or wetlands, which
eventually flow into coastal waters.
To specifically assess the chemical and ecological impacts of sewage pollution in the
BRC and on the fringing reefs around Tobago, we undertook a water quality and coral reef
monitoring project in 2001. The project involved two rounds of sampling -- April-June (dry
season) and September-October (wet season) – to allow monitoring of seasonal effects, including
that of the Orinoco River floodwater plume, which impacts Tobago’s coastal waters during the
wet season (Laydoo, 1991; Risk et al., 1992). Measured variables included: water-column
dissolved inorganic nitrogen (DIN; ammonium and nitrate+nitrite), soluble reactive phosphorus
(SRP), and chlorophyll a (Chl a); macroalgal tissue carbon (C), nitrogen (N), phosphorus (P),
and stable N isotope (δ15N) ratios; and benthic biotic cover (hard corals, octocorals, macroalgae,
turf algae, coralline algae, and sponges). δ15N in benthic macroalgae was used to discriminate
among natural (N-fixation) and anthropogenic (e.g. sewage) N sources fueling algal blooms and
eutrophication in the study area.
2. Materials and methods
2.1 Study sites and sampling rationale
To assess the effect of land-based nutrient discharges on near-shore benthic community
structure, six reef sites in the BRC were sampled along an inshore to offshore gradient (Fig. 1).
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In the inner BRC nearest shore were Princess Reef, just offshore of the house where Princess
Margaret once honeymooned, and Buccoo Point near Buccoo Village, where a sewage outfall is
located; in the mid-BRC were Walkabout Reef, where glass-bottom boat tour operators allow
people to disembark and walk on the back reef (Fig. 2A), and Nylon Pool, where seagrass beds
have taken root in recent decades (Fig. 2D); and, in the outer BRC farthest from shore were
Coral Gardens and Outer Buccoo Reef (Fig. 1). We predicted that the inner BRC sites would
show the strongest evidence of nutrient enrichment from land-based runoff and that there would
be decreasing impact with increasing distance from shore. In addition, a variety of fringing reefs
(FRs) around Tobago’s Caribbean and Atlantic coasts were sampled, including some well known
dive sites: Mt. Irvine “Wall”, the Maverick (a sunken ship-artificial reef), Diver’s Dream, Hilton
reef offshore of the hotel (now, the Tobago Vanguard Hotel), Diver’s Thirst, Culloden, Arnos
Vale, Englishman’s Bay, Three Sisters, and two sites off Little Tobago Island: Kelliston Drain
and Black Jack Hole (Fig. 1). We hypothesized that nutrient enrichment would be relatively
minimal off Little Tobago Island, the site furthest offshore, in the oceanic “blue water” of the
Guyana Current; conversely, greater nutrient enrichment would occur on the FRs more directly
impacted by land-based runoff from the urbanized areas of southwest Tobago, including the six
sites in the BRC as well as the FRs off the Hilton Hotel, Mt. Irvine, the Maverick, Diver’s Dream
and Diver’s Thirst. All sites were sampled in both the dry and wet seasons of 2001 (see rainfall
data, Fig. 3) to assess the effect of stormwater runoff on the seasonal variability of nutrient
concentrations, δ15N, and benthic community structure.
2.2 Analysis of seawater for DIN, SRP, and Chl a
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SCUBA divers collected water samples from the various reef sites between April 10 and
June 20, 2001 (dry season), and between September 24 and October 23, 2001 (wet season).
Water temperatures and depths at the reef sites were measured using Oceanic Datamax Pro
Plus™ dive computers. Divers used clean, 0.5 liter HDPE Nalgene bottles to collect replicate (n
= 4) seawater samples ~ 0.5 m off the bottom at each reef site. Water samples were held on ice
in the dark until return to shore where aliquots were filtered through 0.45 m Whatman GF/F
filters. Loaded filters and filtered samples were then frozen for shipment to analytical labs where
they were analyzed within 30 days of collection. Water samples were analyzed for ammonium,
nitrate + nitrite (referred to simply as nitrate hereafter), and SRP at one of two labs: dry season
samples were analyzed at the Harbor Branch Environmental Laboratory (HBEL) in Ft. Pierce,
FL, whereas wet season samples were analyzed at Nutrient Analytical Services, Chesapeake
Biological Laboratory, University of Maryland System, Solomons, MD (NAS-CBL). The HBEL
samples were analyzed on a Bran and Luebbe TRAACS 2000 Analytical Console (nitrate +
nitrite) and an Alpkem nutrient autoanalyzer (ammonium, nitrite, SRP), with detection limits of
0.08 µM for ammonium, 0.05 µM for nitrate + nitrite, 0.003 µM for nitrite, and 0.01 µM for
SRP. The NAS-CBL samples were analyzed on a Technicon Auto-Analyzer II (nitrate, SRP)
and a Technicon TRAACS 800 (ammonium, nitrite), with detection limits of 0.21 µM for
ammonium, 0.01 µM for nitrate + nitrite, 0.01 µM for nitrite, and 0.02 µM for SRP (D’Elia et
al., 1997). A modified f-ratio (nitrate/DIN) was used to gauge the relative abundance of nitrate
vs ammonium in the DIN pool (McCarthy et al., 1975; Harrison et al., 1987). Salinity was
measured to within ± 1 ‰ using a Bausch and Lomb refractometer. The GF/F filters used for
filtering the water samples were analyzed for Chl-a by extraction in 10 ml of dimethyl sulfoxide
for 30 minutes, then overnight at 5 ˚C with an added 15 ml of 90% acetone. Sample extracts
7
were measured fluorometrically, before and after acidification, to determine Chl-a concentration.
Fluorescence measurements were made using a Turner Designs 10-000R fluorometer equipped
with an infrared-sensitive photomultiplier, calibrated using a pure Chl-a standard.
2.3 Analysis of macroalgae for C:N:P and 15N
SCUBA divers collected replicate (n = 2) composite macroalgae samples from each reef
site in nylon mesh bags. For each species sampled, 3-6 separate plants were collected for each
composite sample to ensure representativeness. Immediately following collection, macroalgae
were cleaned of debris and transferred to plastic zipper-lock bags and held in a cooler above ice
in the dark for transport to the lab. In the lab, the samples were identified, rinsed briefly (3-5 s)
in de-ionized water to remove salt and remaining debris, and placed in plastic dishes for drying
in a lab oven at 65 ˚C for 48 h. Dried macroalgae were ground to a fine powder, using a mortar
and pestle, and stored in sealed plastic vials for shipment. δ15N (‰) analyses were performed at
Isotope Services, Los Alamos, NM, using a Carlo-Erba N/A 1500 Elemental Analyzer and a VG
Isomass mass spectrometer, using Dumas combustion; N2 in air was the standard. δ15N (‰)
values were calculated: δ15N = [(Rsample/Rstandard) – 1] x 103; where R = 14N / 15N. Dry
season macroalgal tissue C, N, and P (%) analyses were performed at NAS-CBL, where C and N
were measured on an Exeter Analytical, Inc., CE-440 Elemental Analyzer, and P was measured
following the methodology of Asplia et al. (1976) using a Technicon Autoanalyzer II (D’Elia et
al., 1997).
2.4 Benthic biotic cover
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At each site, SCUBA divers used an underwater digital video camcorder (Sony TRV 900
in an Amphibico Navigator housing, 100 degree spherical lens) to record imagery along two,
replicate, 50 m belt transects by holding the camcorder perpendicular to the reef surface (0.5 m
off bottom, 0.4 m-2 image area) while slowly swimming along the transects. A second, close-up,
oblique video transect was also recorded to facilitate algal taxa identification and to resolve finescale (1-5 cm) changes in biotic composition in these diverse and often multi-layered
communities. The digital video images were analyzed on a high resolution color monitor using
the random point-count method. This method provides a relatively unbiased estimate of the
benthic cover (%) of hard corals, macroalgae (> 2 cm tall), algal turf (< 2 cm tall), coralline
algae, sponges, and octocorals (Lapointe and Thacker, 2002). Two independent scorers used the
point-count method (with ten randomized dots superimposed over the video image) to score ten
randomly selected images from each 50 m reef transect (200 point counts/reef site x 2 scorers =
400 total point counts per reef site).
2.5 Satellite remote sensing
Tobago is not isolated, but is affected by the Orinoco and Amazon rivers (Hu et al.,
2004b). To help determine whether the study sites were primarily impacted by local discharges
or by the Orinoco River plume, data from the MODIS (MODerate resolution Imaging
Spectroradiometer) instrument onboard the satellite Terra (1999-present) were analyzed. Level1 data for 2001 were obtained from the NASA Goddard Space Flight Center (GSFC), and
processed using the default algorithms in the software package SeaDAS (version 5.1).
Calibrated radiance data were corrected for atmospheric effects and solar/viewing geometry, then
used in a blue/green band-ratio algorithm (O’Reilly et al., 2000) to estimate surface water Chl-a
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concentrations (mg m-3). The underlying assumption was that the blue light was modulated
primarily by phytoplankton. However, because most (> 80-90%) of the blue-light absorption
was due to chromophoric (colored) dissolved organic matter (CDOM) in the Gulf of Paria and
adjacent waters (especially in the Orinoco River plume; Odriozola et al., 2007), such derived
“Chl-a” was only used as a color index to show the spatial patterns of the different water masses,
including the Orinoco River plume. In contrast, the MODIS fluorescence line height (FLH)
product, derived from the red bands using a baseline subtraction algorithm (Letelier et al., 1996),
was nearly immune to CDOM influence (Hu et al., 2005). Hence, FLH was used as a better
index to show spatial biomass patterns.
2.6 Statistical Analyses
Statistical analyses were performed in SPSS 11 for Mac (www.spss.com) using the
Generalized Linear Model (GLM; Type III sum of squares) and Tukey’s HSD (THSD) post hoc
tests. The GLM ANOVA was used to assess differences between samplings (df = 1) and
between the BRC and FR groups (df = 1), and to determine if significant differences existed
among sites (df > 1). If differences among sites were determined by GLM to be significant, then
THSD multi-comparison tests were performed to identify the source(s) of the difference(s).
Differences were considered significant at p ≤ 0.05.
3. Results
3.1 Seawater DIN, SRP, Chl a, and Salinity
DIN concentrations (Fig. 4) averaged 1.6 ± 1.1 µM (n = 107) overall and varied both
temporally (p < 0.001) and spatially (p = 0.005) among the sites. Mean DIN (sites pooled) was
10
lower (p < 0.001) in the dry season (0.7 ± 0.5 µM; n = 51) than in the wet season (2.4 ± 0.7 µM;
n = 56). The seasonal DIN increase was mostly the result of a 4-fold ammonium increase (p <
0.001) from the dry season (0.4 ± 0.2 µM; n = 51) to the wet season (1.6 ± 0.6 µM; n = 56).
Nitrate increased (p < 0.001) 3-fold from the dry season (0.3 ± 0.4 µM; n =51) to the wet season
(0.9 ± 0.5 µM; n = 56) but was a relatively minor component of the DIN pool compared to
ammonium in both seasons, as indicated by consistently low f-ratios (0.32-0.35). The mean DIN
in the BRC was higher (p = 0.012) than at the FRs in the dry season (0.9 ± 0.5 µM vs. 0.5 ± 0.4
µM) but not in the wet season (2.4 µM vs. 2.5 µM). Lowest mean concentrations of both DIN
(1.0 ± 1.1) and ammonium (0.7 ± 0.7) occurred at Black Jack Hole, whereas the highest DIN (2.4
± 0.7 µM) and ammonium (2.0 ± 0.9 µM) occurred at Buccoo Point in the inner BRC.
SRP concentrations (Fig. 5) averaged 0.23 ± 0.15 (n = 107) overall and varied temporally
(p = 0.034) and spatially (p < 0.001). The mean SRP concentration (sites pooled) was higher (p
= 0.011) in the dry season (0.26 ± 012 µM; n = 51) than in the wet season (0.20 ± 0.17 µM; n
=56). Mean SRP concentrations at the BRC sites were not significantly different than those at
the FRs, either overall or during the dry or wet seasons. The lowest SRP concentrations occurred
at Black Jack Hole (0.18 ± 0.09 µM), and the highest occurred at Buccoo Point (0.50 ± 0.61
µM), significantly higher (p < 0.014) than all other sites.
DIN:SRP ratios (Fig. 5) averaged 9 ± 7 (n = 51) during the study and varied both
temporally and spatially. Overall, the mean DIN:SRP ratio was higher (p < 0.001) in the wet
season (14 ± 4; n = 56) than in the dry season (3 ± 3; n = 51). The DIN:SRP ratio was higher (p
< 0.001) in the BRC (4 ± 3; n = 20) than on the FRs (2 ± 3; n = 31) in the dry season. However,
wet season DIN:SRP was higher (p = 0.008) on the FRs (15 ± 4; n = 44) than in the BRC (12 ±
4; n = 26).
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Chl a (Fig. 6) averaged 0.32 ± 0.19 µg/l at all stations throughout the study and varied
temporally (p = 0.038) and spatially (p = 0.031). Overall, Chl a averaged 0.28 ± 0.02 µg/l (n =
51) in the dry season and 0.35 ± 0.17 µg/l (n = 70) in the wet season (sites pooled). The lowest
value was at Coral Gardens (0.09 ± 0.02 µg/l) in the dry season and the highest was in the Bon
Accord Lagoon (1.13 ± 0.16 µg/l) in the wet season. Dry season Chl a values were similar
between the BRC (0.23 ± 0.22 µg/l) and the FRs (0.31 ± 0.22 µg/l), whereas wet season Chl a
was higher (p = 0.031) in the BRC (0.41 ± 0.24 µg/l) than on the FRs (0.32 ±0.10 µg/l).
Salinity varied spatially and seasonally throughout the study. In the dry season, salinity
in the middle and outer BRC ranged 36-37 ‰, with lower values at Buccoo Point reef ranging
31-36 ‰; on the FRs, salinity ranged 36-37 ‰. In the wet season, salinity in the BRC ranged
34-36 ‰, and on the FRs salinity stratification was evident, with lower salinities of 34-36 ‰ in
the surface layer compared to 36-38 ‰ in the near-bottom layer at most sites.
3.2 C:N:P and δ15N in macroalgae
Macroalgae in the BRC were enriched in N but not P compared to the FRs during the dry
season (Table 1). The mean C:N (16 ± 6; n = 16) in the BRC was lower (p = 0.014) than on the
FRs (21 ± 7; n = 24), in contrast to the mean C:P values, which were statistically similar (770 ±
294 in BRC vs 759 ± 385 on the FRs). These changes co-occurred with a higher (p = 0.002)
N:P ratio in the BRC (50 ± 16; n = 16) compared to the FRs (35 ± 12; n = 24). The lowest C:N
ratio (8) occurred at Buccoo Point in the BRC, the highest (26) at Black Jack Hole off Little
Tobago Island. The lowest C:P (444) also occurred at Buccoo Point but the highest (1238)
occurred at Coral Gardens in the outer BRC. The lowest N:P (28) occurred at Kelliston Drain
off Little Tobago Island, the highest (62) at Coral Gardens in the BRC.
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Macroalgal 15N values (Fig. 7) averaged + 5.9 ± 1.2 ‰ (n = 174) throughout the study
and varied temporally, spatially, and by taxa. The mean 15N in the dry season (+ 5.5 ± 1.2 ‰;
n = 82) was lower (p = 0.01) than it was in the wet season (+ 6.1 ± 1.2 ‰; n = 92). Overall (sites
pooled) mean 15N was lower (p < 0.001) on the FRs (+5.5 ± 1.3 ‰; n = 94) than it was in the
BRC (+6.2 ± 1.1 ‰; n = 80). The lowest 15N values occurred at Black Jack Hole (+ 2.9 ‰)
and the highest were at Princess Reef (+7.3 ‰) in the inner BRC. Taxonomically, the highest
15N values (~ + 12 ‰) were found in the chlorophyte Ulva lactuca and in the rhodophytes
Gracilaria tikvahiae and Agardhiella subulata, nutrient indicator species collected adjacent to
the sewage outfall near Buccoo Point (Fig. 7; Table 1). 15N values varied significantly (p <
0.001) among macroalgae classes (divisions), with highest values in the rhodophytes (+7.0 ± 2.3
‰; n = 30), followed by the chlorophytes (+ 6.2 ± 1.3 ‰; n = 82), and the phaeophytes (+ 5.5 ±
1.2 ‰; n = 54).
3.3 Benthic biotic cover
The inner BRC sites had distinctly higher macroalgal cover and lower coral cover than
elsewhere in the study area (Fig. 8). The highest macroalgal cover (up to 40%) occurred at
Princess Reef and Buccoo Point where blooms of Halimeda opuntia, Bryopsis spp., and
Caulerpa spp. occurred (Fig. 2B; Table 1). Coral cover was < 10% at these two sites, compared
to 20-40% at coral cover at the outer BRC sites (Coral Gardens, Outer Reef) comprised of the
genera Acropora, Montastrea, Diploria, and Siderastrea. Algal turf was a major component of
reef communities in the BRC, with cover ranging up to ~ 50%. The zoanthid Palythoa
caribaeorum was another significant component of the BRC reef communities and ranged up to
> 20% cover at Buccoo Point where it overgrew dead coral skeletons (Fig. 2C). Compared to the
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BRC, the FRs had consistently higher hard coral cover (ex. > 45% at Culloden Reef), including
the plate-form of Montastrea annularis and species of coralline algae (up to ~ 40% cover), but
generally low (< 10%) frondose macroalgae cover.
4. Discussion
Our water column nutrient data from Tobago are the first to document the role of landbased nitrogen runoff in eutrophication on the island’s fringing coral reefs. Previous studies in
Trinidad & Tobago have emphasized the role of phosphorus pollution from industrial and
domestic wastewaters (Kumarsingh et al., 1998a, b). However, the relatively high background
SRP concentrations throughout the entire study area (~ 0.23 M) are greater than reported for
coastal waters in the Caribbean region (Rajendran et al., 1991; Lapointe, 2004) and, combined
with relatively low DIN:SRP ratios (< 15:1), suggest N rather than P limitation of algal growth.
Such high background SRP concentrations, low DIN:SRP ratios, and a tendency towards Nlimitation are indicative of siliciclastic environments; this contrasts with the carbonate-rich
environments in Jamaica, the Bahamas, and the Florida Keys where low SRP concentrations and
high DIN:SRP ratios support strong P-limitation (Lapointe et al., 1992). Hence, the natural
volcanic geology of Tobago may pre-dispose its coastal waters to nitrogen rather than to
phosphorus limitation.
The differential effects of carbonate-rich vs. siliciclastic geology on N vs P availability in
Tobago is apparent in our data from the BRC and the FRs. Although the extensive limestone
formation surrounding the Buccoo Reef provides a sink for natural and anthropogenic SRP
through adsorption (Berner and Morse, 1974; DeKanel and Morse, 1978), such is not the case for
DIN (Lapointe et al., 1990). Ammonium was highly enriched in coastal waters of Tobago in the
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wet season of this study, consistent with reports of elevated ammonium in coastal waters of the
Florida Keys in the wet season (Lapointe et al., 2004) and, more generally, in the wakes of
Caribbean islands (Corredor et al., 1984). This phenomenon explains how relatively high N:P
ratio inputs from the Buccoo Reef watershed results in higher water column DIN:SRP and
macroalgal N:P ratios in the BRC compared to the FR. The elevated DIN:SRP ratios in the BRC
were most pronounced during the wet season, when wastewater loads from “soak-aways” and
other sources on the watershed are maximal. Such high N:P inputs lead to P-limitation of
primary production in carbonate-rich coastal waters (Lapointe, 1987) and explains why many
Caribbean coastal waters are limited primarily by P rather than N (Lapointe et al., 1992;
Corredor et al., 1999). The reduced “limestone” effect at the FRs, relative to the BRC, results in
lower DIN:SRP and N:P ratios, and a shift to more N-limited primary production.
Multiple lines of evidence from our study indicate that Buccoo Point – directly impacted
by wastewater discharges from the adjacent upland watershed -- was the most nutrient impacted
site during our study. The highest water-column DIN, ammonium, and SRP concentrations of
the entire study occurred there, along with the lowest macroalgal C:N and C:P ratios of the study,
demonstrating the impacts of elevated water column DIN and SRP concentrations on reef biota.
These observations are consistent with previous research using cylindrical cores of the coral
Montastrea annularis, in the BRC vs Culloden reef, to compare historical trends in P availability
(Kumarsingh et al., 1998b). Those researchers found higher fractions of organic P in the coral
cores in the BRC than Culloden reef, and that temporal patterns of increase in both total and
organic P in the BRC coral cores correlated positively with human activities on the watershed.
Our results also support previous findings by the Institute of Marine Affairs, Trinidad (IMA,
1996) that the highest nutrient concentrations in southwest Tobago occurred in Buccoo Bay and
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the Bon Accord Lagoon, both of which have experienced increasing wastewater nutrient
loadings in recent decades.
The effects of elevated nutrient concentrations and high DIN:SRP ratios in the BRC were
evidenced in increased biomass and elevated tissue N and P contents of macroalgae in the BRC
compared to the FRs. Macroalgae in the BRC, enriched in N compared to the FRs, had lower
C:N (15 vs 21) and higher N:P (50 vs 35) ratios as a result. The lower C:N ratios reflect reduced
N-limitation of growth and explains the overall higher macroalgal biomass in the BRC compared
to the FR. The relatively high N enrichment in the BRC drives the macroalgae to greater Plimitation, as evidenced by the higher N:P ratio of macroalgae in the BRC compared to the FRs.
Blooms of the chlorophytes Bryopsis spp., Caulerpa spp., and Halimeda opuntia were observed
overgrowing reefs in the BRC (Fig. 2B), a phenomenon that was not observed at any of the FRs.
Turtle grass, Thalassia testudinum, invaded the carbonate sands at Nylon Pool (Fig. 2D) over a
decade ago, another symptom of sewage-driven eutrophication in oligotrophic coral reef regions
(Bell, 1992). The phenomenon by which high N:P inputs from the watershed drive macroalgal
blooms (and seagrass growth) on coral reefs towards increased P-limitation has been reported for
other carbonate-rich waters in the Caribbean, including the Florida Keys (Lapointe, 1987;
Lapointe and Clark, 1992; Lapointe et al., 2004), southeast Florida (Lapointe et al., 2005a),
Jamaica (Lapointe, 1997; Lapointe and Thacker, 2002), Martinique (Littler et al., 1992), and
Bermuda (Lapointe and O’Connell, 1989).
The identification of wastewater as the source of DIN enrichment in the BRC was
apparent from the elevated macroalgal 15N in the BRC compared to the FRs. Numerous
studies have shown how macroalgal 15Nvalues faithfully discriminate among various natural
and anthropogenic nitrogen sources (see Risk et al., 2009 for a review). For example, France et
16
al. (1998) showed that 21 species of tropical macroalgae in coastal waters of southwestern Puerto
Rico had a mean 15Nof + 0.3 ± 1.0 ‰, a value close to the atmospheric signature of 0 ‰ and
indicative of N-fixation. In contrast, macroalgae exposed to varying degrees of urban
wastewater pollution in Negril, Jamaica (Lapointe and Thacker, 2002), southeast Florida
(Lapointe et al., 2005b), the Florida Keys (Lapointe et al., 2004), and Moreton Bay, Australia
(Costanzo et al., 2001) all reported 15N values ranging from ~ + 3 to + 15 ‰, with values > 8
‰ in close proximity to wastewater sources. This pattern is consistent with our results, where
the highest 15N values (~ + 12 ‰) were observed in the “nutrient indicator” species (Ulva
lactuca, Gracilaria tikvahiae, Agardhiella subulata) near the wastewater outfall in Buccoo Bay.
Lower mean values of + 7.3 ‰ for Princess Reef, in the inner BRC, and + 6.2 ‰ for macroalgae
throughout the BRC would be expected from dilution of wastewater N from the inner to the outer
BRC. These 15Ndata support the hypothesis that the entirety of the BRC has been
significantly impacted by wastewater DIN from submarine groundwater discharge (SGD) of
leachate from “soak-aways” and from direct sewage outfall discharges. Lower, but relatively
elevated 15Nvalues occurred in macroalgae at other reef sites in southwest Tobago, especially
off the Hilton Hotel downstream of Scarborough, indicating widespread sewage DIN enrichment
downstream of urban areas. The lowest 15N value, (+ 2.5 ‰), measured during the dry season
at Black Jack Hole, off Little Tobago Island, was more characteristic of an oligotrophic system
less impacted by human activity although, even there, 15N values increased significantly during
the wet season as a result of more widespread dispersion of land-based sewage pollution via
increased stormwater runoff and SGD.
Elevated Chl a concentrations during the wet season provides further evidence of
watershed-driven eutrophication in the BRC. In both seasons, maximum Chl-a correlated with
17
decreased DIN concentrations, but not with SRP. This pattern results from rapid uptake by
phytoplankton of DIN, the primary limiting nutrient in coastal waters subject to sewage
pollution. These findings support previous observations in Kaneohe Bay, Hawaii (Laws and
Redalje, 1979) and the Florida Keys (Lapointe and Clark, 1992) where Chl a provided a good
“integrated” index of eutrophication in tropical and subtropical coastal waters. The generally
low DIN concentrations on Tobago’s fringing reefs (< 0.3 M), especially off Little Tobago
Island, not only limits phytoplankton biomass, but also the growth of macroalgae. Mean DIN
concentrations > 0.5 M are needed to support “blooms” of benthic macroalgae (Lapointe,
1997), such as those we observed on reef sites in the inner BRC. Classic “indicator” species of
nutrient enrichment, including the rhodophytes Gracilaria tikvahiae and Agardhiella subulata,
and the chlorophytes Ulva lactuca, Halimeda opuntia, Bryopsis spp, and Caulerpa racemosa
were abundant on reefs in the inner BRC where DIN concentrations were > 0.5 M, especially
near the sewage outfall in Buccoo Bay. In contrast, macroalgae were generally less abundant on
the fringing reefs around Tobago that had lower DIN concentrations. Similar macroalgal
zonation patterns resulting from land-based nutrient gradients have been noted on other islands
in the Caribbean region, including Jamaica (Lapointe, 1997; Lapointe and Thacker, 2002), the
Florida Keys (Lapointe et al., 2004) and the Turks and Caicos Islands (Goreau et al., 2008).
The MODIS image series added additional evidence to differentiate the origin of elevated
nutrients and phytoplankton biomass. The synoptic water circulation patterns in the color
imagery often revealed land-reef connectivity that could complement the in situ data (e.g.,
Andréfouët et al., 2002; Hu et al., 2004a; Soto et al., 2009). Figure 9 shows several examples of
the MODIS “Chl” and FLH images during both the dry and wet seasons. While the “Chl a”
images clearly showed the influence of the Orinoco River plume in the nearshore waters of
18
Tobago (the green-yellow-red colors) during the wet season, the corresponding FLH images
suggested that this influence was primarily through CDOM, as opposed to phytoplankton
biomass. The absence of elevated phytoplankton biomass in the Orinoco River plume near
Tobago suggested that riverine nutrients were depleted by the time the plume reached Tobago.
Similarly, Ryther et al. (1967) compared Amazon outflow water with surrounding seawater and
reported very low levels of dissolved nutrients and phytoplankton in this lower salinity plume.
Hence, we conclude that the elevated nutrient and Chl a concentrations in the BRC and on the
FRs during the wet season were primarily of local origin, rather than from the Orinoco River
outflow (Fig. 2E).
The loss of hard coral cover and its replacement by macroalgae on Jamaican coral reefs
over the past two decades has been repeatedly attributed to the “top-down” effects of overfishing
of herbivorous fish stocks and die-off of the long-spined urchin Diadema (Hughes, 1994;
Jackson et al., 2001). However, similar losses of hard corals and increases in macroalgal blooms
have occurred over the past two decades in the BRC, a Marine Protected Area with an abundant
herbivore population of parrotfish (including large adults), surgeonfish, and chubs. However, as
described here, the BRC has also been polluted by land-based sewage inputs. The most sewage
impacted inshore reef in the BRC (Princess Reef) not only had abundant macroalgae (Caulerpa,
Halimeda; Fig 2C) but also dense populations of sea urchins (Echinometra viridis). These
observations point to “bottom-up” control (i.e. nutrients) of not only the macroalgal biomass, but
the echinoid populations as well. Hunter and Price (1992) suggested that a “bottom-up template”
is the most realistic approach for understanding trophic dynamics in ecosystems because plants
have obvious primacy in food webs. We concur and suggest that sewage nitrogen subsidies over
recent decades have increased both macroalgae and grazer populations (echinoids and
19
herbivorous fishes) in the BRC, as growth of marine herbivores is typically limited by dietary
nitrogen (Mattson, 1980). Reef health, biodiversity and ecological services have been reduced
by sewage-driven eutrophication in the BRC despite abundant grazer populations.
In summary, our results support the conclusion of Siung-Chang (1997) for the Caribbean
region, and of Agard & Gobin (2000) for Trinidad & Tobago, that the most important source of
marine pollution is domestic sewage, which appears to be impacting not only the BRC but also
other fringing coral reefs “downstream” of Tobago’s populated southwest coast.
Acknowledgements
We gratefully acknowledge Mr. Rae De Beer and the World of Watersports (Caribbean),
Ltd for providing boat support on the Atlantic Blues that made this research possible. This
research was supported by the Buccoo Reef Trust, the Harbor Branch Oceanographic Institution,
Inc., and the U.S. NASA Ocean Biology and Biogeochemistry (OBB) program. This is
contribution number 1788 from the Harbor Branch Oceanographic Institute at Florida Atlantic
University, Ft. Pierce, FL.
20
References
Agard, J.B.R., Gobin, J.F., 2000. The Lesser Antilles, Trinidad and Tobago. In: Sheppard, C.
(Ed.), Seas at The Milleneum: An Environmental Evaluation. Volume I. Regional Seas:
Europe, The Americas and West Africa. Elsevier, New York. pp. 627-641.
Andréfouët S., Mumby, P.J., McField, M., Hu, C., and Muller-Karger, F. E., 2002. Revisiting
coral reef connectivity. Coral Reefs. 21:43-48.
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.
Banner, A.H., 1974. Kaneohe Bay, Hawaii, urban pollution and a coral reef ecosystem. Proc.
2nd Int. Symp. Coral Reefs, 2, 685-702.
Barile, P.J., Lapointe, B.E., 2005. Atmospheric nitrogen deposition from a remote source
enriches macroalgae in a coral reef ecosystem at Green Turtle Cay, Abacos, Bahamas.
Mar. Poll. Bull. 50, 1262-1272.
Bell, P.R.F., 1992. Eutrophication and coral reefs: some examples in the Great Barrier Reef
Lagoon. Wat. Res. 26, 89-93.
Berner, R.A., Morse, J.W., 1974. Dissolution kinetics of calcium carbonate in sea water; IV,
Theory of calcite dissolution. Amer. J. Sci. 274, 108-134.
Corredor, J. E., Morrel, J., Mendez, A. 1984. Dissolved nitrogen, phytoplankton biomass and
island mass effects in the northeastern Caribbean Sea. Carib. J. Sci. 20(3-4), 129-137.
Corredor, J.E., Howarth, R.W., Twilley R.R., and M.M Morell. 1999. Nitrogen Cycling and
Anthropogenic Impact in the Tropical Interamerican Seas. Biogeochem. 46, 163-178.
21
Costa, O.S., Jr., Leao, Z.M.A.N., Nimmo, M., Attrill, M.J., 2000. Nutrification impacts on coral
reefs from northern Bahia, Brazil. Hydrobiologia 440, 307-315.
Costanzo, S.D., O'Donohue, M.J., Dennison W.C., Loneragan N.R., Thomas, M., 2001. A New
Approach for Detecting and Mapping Sewage Impacts. Mar. Poll. Bull. 42, 149-156.
DeKanel, J., Morse, J.W., 1978. The chemistry of orthophosphate uptake from seawater onto
calcite and aragonite. Geochim. Cosmochim. A. 42, 1335-1340.
D’Elia, C.F., Connor, E.E., Kaumeyer, N.L., Keefe, C.W., Wood, K.V., Zimmerman, C.F., 1997.
Nutrient analytical services: standard operating procedures. Technical Report Series No.
158-97, Chesapeake Biological Laboratory, Solomons, MD.
France, R., Holmquist, J., Chandler, M., Cattaneo, A., 1998. 15N evidence for nitrogen fixation
associated with macroalgae from a seagrass-mangrove-coral reef ecosystem. Mar. Ecol.
Progr. Ser. 167, 297-299.
Goreau, T. J., T. Fisher, F. Perez, K. Lockhart, M. Hibbert, and A. Lewin. 2008. Turks and
Caicos Islands 2006 coral reef assessment: Large-scale environmental and ecological
interactions and their managemenent implications. Revista Biologia Tropical 56, 25-49.
Harrison, W.G., Platt, T., Lewis, M.R., 1987. The f-ratio and its relationship to ambient nitrogen
concentration in coastal waters. J. Plankton Res. 9, 235-248.
Hu, C., Hackett, K.E., Callahan, M.K., Andréfouët, S., Wheaton, J.L., Porter, J.W., and MullerKarger, F.E., 2003. The 2002 ocean color anomaly in the Florida Bight : a cause of local
coral reef decline? Geophys. Res. Lett. 30(3), 1151, doi:10.1029/2002GL016479.
Hu, C., Muller-Kager, F.E., Vargo, G.A., Neely, M.B., and Johns, E., 2004a. Linkages between
coastal runoff and the Florida Keys ecosystem: A study of a dark plume event. Geophys.
Res. Lett. 31, L15307, doi:10.1029/2004GL020382.
22
Hu, C., Montgomery, E., Schmitt, R., Muller-Karger, F.E., 2004b. The Amazon and Orinoco
River plumes in the tropical Atlantic: Observation from space and S-Floats. Deep Sea
Res-II 51, 1151-1171.
Hu, C., Muller-Karger, F.E., Taylor, C., Carder, K.L., Kelble, C., Johns, E., Heil C., 2005. Red
tide detection and tracing using MODIS fluorescence data: A regional example in SW
Florida coastal waters. Remote Sens. Environ. 97, 311-321.
Hughes, T.P., 1994. Catastrophes, phase-shifts, and large-scale degradation of a Caribbean coral
reef. Science 265, 1547-1551.
Hunter, M.D., Price, P.W., 1992. Playing chutes and ladders: heterogeneity and the relative roles
of bottom-up and top-down forces in natural communities. Ecology 73, 724-732.
IMA, 1994. The formulation of a management plan for the Buccoo Reef Marine Park, Vol. 3:
Biological investigations and water quality monitoring. Document prepared for the
Tobago House of Assembly. Institute of Marine Affairs, Trinidad.
IMA, 1996. Report of phase I: An assessment of the biophysical environment of southwest
Tobago. Document prepared for the Organization of American States. Technical Report,
Institute of Marine Affairs, Trinidad.
Jackson, J.B.C., Kirby, M.X., Berger, W.H., Bjorndal, K.A., Botsford, L.W., Bourque, B.J.,
Bradbury, R.H., Cooke, R., Erlandson, J., Estes, J.A., Hughes, T.P., Kidwell, S., Lange,
C.B., Lenihan, H.S., Pandolfi, J.M., Peterson, C.H., Steneck, R.S., Tegner, M.J., Warner,
R.W., 2001. Historical overfishing 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.J.F.,
Johannes, R.E. (Eds.), Tropical Marine Pollution, Elsevier, Oxford, pp. 13-51.
23
John, G.M., 1996. Quantitative characteristics of land-based sources of marine pollution in the
vicinity of the Buccoo Reef Marine Park, Tobago. MS Thesis, University of the West
Indies, Department of Biology, Cave Hill Campus, Barbados.
Kenny, J.S., 1976. A preliminary study of the Buccoo Reef/ Bon Accord Complex with special
reference to development and Management. Department of Biological Sciences,
University of the West Indies, St. Augustine.
Kumarsingh, K., Hall, L.A., Siung-Chang, A.M., Stoute, V.A., 1998a. Phosphorus in sediments
of a shallow bank influenced by sewage and sugar factory effluents in Trinidad, West
Indies. Mar. Poll. Bull. 36, 185-192.
Kumarsingh, K., Laydoo, R., Chen, J.K., Siung-Chang, A.M., 1998b. Historic records of
phosphorus levels in the reef-building coral Montastrea annularis from Tobago, West
Indies. Mar. Poll. Bull. 36, 1012-1018.
Lapointe, B.E., 1987. Phosphorus- and nitrogen-limited photosynthesis and growth of
Gracilaria tikvahiae (Rhodophyceae) in the Florida Keys: An experimental field study.
Mar. Biol. 93, 561-568.
Lapointe, B.E., 1997. Nutrient thresholds for bottom-up control of macroalgal blooms on coral
reefs in Jamaica and southeast Florida. Limnol. Oceanogr. 42, 1119-1131.
Lapointe, B.E., 2004. Phosphorus-rich waters at Glovers Reef, Belize? Mar. Poll. Bull. 48, 193195.
Lapointe, B.E., Clark, M.W., 1992. Nutrient inputs from the watershed and coastal
eutrophication in the Florida Keys. Estuaries 15, 465-476.
24
Lapointe, B.E., O'Connell, J., 1989. Nutrient-enhanced growth of Cladophora prolifera in
Harrington Sound, Bermuda: Eutrophication of a confined, phosphorus-limited marine
ecosystem. Estuar. Coast. Shelf S. 28, 347-360.
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,
pp. 939-963.
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, 23-58.
Lapointe, B.E., Littler, M.M., Littler, D.S., 1992. Nutrient availability to marine macroalgae in
siliciclastic versus carbonate-rich coastal waters. Estuaries 15, 75-82.
Lapointe, B.E., O’Connell, J.D., Garrett, G.S., 1990. Nutrient couplings between on-site sewage
disposal systems, groundwaters, and nearshore surface waters of the Florida Keys.
Biogeochem. 10, 289-308.
Lapointe, B.E., Barile, P.J., Littler, M.M., Littler, D.S., 2005b. Macroalgal blooms on southeast
Florida coral reefs: II. Cross-shelf discrimination of nitrogen sources indicates
widespread assimilation of sewage nitrogen. Harmful Algae 4, 1106-1122.
Lapointe, B.E., Barile, P.J., Littler, M.M., Littler, D.S., Bedford, B.J., Gasque, C., 2005a.
Macroalgal blooms on southeast Florida coral reefs: I. Nutrient stoichiometry of the
invasive green alga Codium isthmocladum in the wider Caribbean indicates nutrient
enrichment. Harmful Algae 4, 1092-1105.
25
Laws, E.A., Redalje, D.G., 1979. Effects of sewage enrichment on the phytoplankton population
of a sub-tropical estuary. Pac. Sci. 33, 129-144.
Laydoo, R.S., 1991. A guide to the coral reefs of Tobago. Institute of Marine Affairs and the
Asa Wright Nature Centre, Rep. of Trinidad & Tobago.
Laydoo, R.S. and Heileman, L., 1987. Environmental impacts of the Buccoo and Bon Accord
Sewage Treatment plants, southwestern Tobago. A preliminary report. Institute of
Marine Affairs and Crusoe Reef Society, Rep. of Trinidad & Tobago.
Letelier, R.M., and Abott, M.R., 1996. An analysis of chlorophyll fluorescence algorithms for
the Moderate Resolution Imaging Spectrometer (MODIS). Remote Sens. Environ. 58,
215-223.
Likens, G.E., 2001. Biogeochemistry, the watershed approach: some uses and limitations. Mar.
Freshwater Res. 52, 5-12.
Littler, M.M., Littler, D.S., Lapointe, B.E., 1992. Modification of tropical reef community
structure due to cultural eutrophication: the southwest coast of Martinique. 7th Int. Coral
Reef Symp., Guam, pp. 335-343.
Mattson, W.J., 1980. Herbivory in relation to plant nitrogen content. Ann. Rev. Ecol. Syst. 11,
119-161.
McCarthy, J.J., Taylor, W.R., Taft, J.L., 1975. The dynamics of nitrogen and phosphorus
cycling in the open waters of Chesapeake Bay. In: Church, T.M. (Ed.), Marine
Chemistry of the Coastal Environment. ACS Symp. Ser. #18, Amer. Chem. Soc.,
Washington, D.C., pp. 664-681.
NRC, 2000. Clean Coastal Waters: Understanding and Reducing the Effects of Nutrient
Pollution. National Research Council, National Academy Press, Washington, D.C.
26
Odriozola, A.L., Varela, R., Hu, C., Astor, Y., Lorenzoni, L., Muller-Karger, F.E., 2007. On the
absorption of light in the Orinoco River plume. Cont. Shelf Res. 27, 1447-1464.
O'Reilly, J.E., Maritorena, S., O'Brien, M.C., Siegel, D.A., Toole, D., Menzies, D., Smith, R.C.,
Mueller, J.L., Mitchell, B.G., Kahru, M., Chavez, F.P., Strutton, P., Cota, G.F., Hooker,
S.B., McClain, C.R., Carder, K.L., Müller-Karger, F., Harding, L., Magnuson, A.,
Phinney, D., Moore, G.F., Aiken, J., Arrigo, K.R., Letelier, R., Culver, M., 2000.
Volume 11, SeaWiFS postlaunch calibration and validation analyses, Part 3. In: Hooker,
S.B., Firestone, E.R. (Eds.), SeaWiFS postlaunch technical report series. NASA/TM2000-206892, Vol. 11, pp. 1-49.
Paerl, H.W., Dennis, R.L., Whitall, D.R., 2002. Atmospheric deposition of nitrogen:
Implications for nutrient over-enrichment of coastal waters. Estuaries 25, 677-693.
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 (1-2), 81-86.
Risk, M.J., Van Wissen, F.A., Beltran, J.C., 1992. Sclerochronology of Tobago corals: a record
of the Orinoco? Proc. 7th Int. Coral Reef Symp. 1, 156-161.
Risk, M.J., Lapointe, B.E., Sherwood, O.A., Bedford, B.J., 2009. The use of 15N in assessing
sewage stress on coral reefs. Mar. Poll. Bull. 58, 793-802.
Ryther, J.H., Menzel, D.W., Corwin, N., 1967. Influence of the Amazon River outflow on the
ecology of the western tropical Atlantic I. Hydrography and nutrient chemistry. J. Mar.
Res. 25, 69-83.
Siung-Chang, A., 1997. A review of marine pollution issues in the Caribbean. Environ.
Geochem. Health 19, 45-55.
27
Smith, S.V., Kimmerer, W.J., Laws E.A., Brock R.E., Walsh, T.W., 1981. Kaneohe Bay sewage
diversion experiment: Perspectives on ecosystem responses to nutritional perturbation.
Pac. Sci. 35, 279-396.
Soto, I., Andrefouet, S., Hu, C., Muller-Karger, F.E., Wall, C.C., Sheng, J., and Hatcher, B.G.,
2009. Physical connectivity in the Mesoamerican Barrier Reef System inferred from 9
years of ocean color observations. Coral Reefs. DOI 10.1007/s00338-009-0465-0.
UNEP, 1994. Regional overview of land based sources of pollution in the wider Caribbean
region. Caribbean Environment Program Technical Report 33. United Nations
Environmental Programme, Caribbean Environment Program, Kingston.
28
Figure Legend
Figure 1. Map, showing Tobago’s location, monitoring site locations on Tobago fringing reefs
(FRs) and in the Buccoo Reef Complex (BRC), and an aerial view of the BRC, looking
SSW.
Figure 2. A.) “Reef walking” in the BRC; B.) blooms of Caulerpa racemosa and Halimeda
opuntia at Princess Reef in the inner BRC; C.) expansion of the zoanthid Palythoa
cariboreum on outer Buccoo Reef; D.) Nylon Pool, showing underwater dark patches
where the turtle grass, Thalassia testudinum, has recently invaded; E.) aerial view of
coastal riverine discharges from Tobago during the wet season.
Figure 3. Monthly rainfall at Crown Point, Tobago, 2001.
Figure 4. Ammonium, nitrate, and DIN concentrations (µM), and f-ratios in the BRC (left) and
on the FRs (right) during the 2001 dry (April-June) and wet (September-October)
seasons. Values represent means ± 1 SD (n = 4 site-1 sampling-1).
Figure 5. Soluble reactive phosphorus (SRP) concentrations (µM) and DIN:SRP ratios in the
BRC (left) and on the FRs (right) during the 2001 dry (April-June) and wet (SeptemberOctober) seasons. Values represent means ± 1 SD (n = 4 site-1 sampling-1).
Figure 6. Chlorophyll-a concentrations (µg/l) in the BRC (left) and on the FRs (right) during the
2001 dry (April-June) and wet (September-October) seasons. Values represent means ±
1 SD (n = 4 site-1 sampling-1).
Figure 7. Macroalgal tissue 15N (‰) in the BRC (left) and on the FRs (right) during the 2001
dry (April) and wet (September-October) seasons. Values represent means ± 1 SD (n =
2-7 site-1, see Table 1).
29
Figure 8. Benthic biotic cover (%) in the BRC (Princess Reef, Buccoo Point, Coral Gardens,
Buccoo Reef) and on the FRs (Arnos Vale, Culloden, Englishman’s Bay, and Three
Sister’s). Values represent means ± 1 SD (n = 4 site-1).
Figure 9. MODIS/Terra imagery showing near-shore waters of Tobago under the influence of the
Orinoco River plume during the wet season (August-October), which is mostly CDOM
rather than chlorophyll-a (Chl-a). Left panels show MODIS “chlorophyll-a”
concentrations (Chl, mg m-3) derived from the color ratio between the blue (443 or 488
nm) and green (551 nm) bands. Because both Chl-a and CDOM strongly absorb the blue
light, Chl-a values actually represent a combined effect of the two. Right panels show
the MODIS chlorophyll fluorescence line height (FLH, mW cm-2 m-1 sr-1), which is
much less affected by riverine CDOM. Despite significant noise (striping, cloud-edge
effect, sun glint effect), the spatial patterns of FLH and their contrast to the left panels
suggest that most of the river plume signal near Tobago are due, not to Chl-a, but to
riverine CDOM.
30
Table Legend.
Table 1. Macroalgal tissue C, N, and P contents (%), and C:N, C:P, and N:P ratios in the BRC
and on FRs around Tobago, April, 2001.
31