Land-Based Nutrient Enrichment of the Buccoo Reef Complex and
Fringing Coral Reefs of Tobago, West Indies
B. E. Lapointe1, R. Langton2, O. Day2, B. Bedford1, C. Hu3 and Arthur Potts4
1
Center for Marine Ecosystem Health, Harbor Branch Oceanographic Institute, 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
Institute for Marine Remote Sensing, College of Marine
Science, University of South Florida, St. Petersburg, FL
33701 U.S.A.
4
Centre for Marine Sciences, Institute of Marine Affairs,
Hill Top Lane, Chaguaramas, P.O. Box 3160, Carenage,
Trinidad and Tobago, W.I.
*Corresponding author; Tel.: 772-465-2400 ext 276; fax: 772-468-0757
e-mail address: lapointe@hboi.edu
Key words: coral reef, macroalgae, eutrophication, sewage, nitrogen, phosphorus,
Orinoco
Abstract
Land-based runoff represents a major source of marine pollution in the Caribbean Sea.
The fringing coral reefs of Tobago, including the Buccoo Reef Complex (BRC), can be
affected locally by wastewater discharges and storm water runoff, as well as regionally
by the floodwaters of the Orinoco River during the wet season. We examined the effects
of land-based nutrient pollution by measuring dissolved water column nutrients (DIN,
SRP), and chlorophyll a, C:N:P and 15N contents of macroalgae, and % cover of coral
and macroalgae at a variety of sites on the Buccoo Reef and fringing reefs (FR) in the dry
(April - June) and wet (September -October) seasons of 2001. Concentrations of DIN
(mostly ammonium) increased at all stations from the dry to wet seasons, in contrast to
SRP that decreased from the dry to wet season. These seasonal shifts in nutrient
concentrations resulted in a significant increase in the DIN:SRP ratio from the dry to wet
season. In April, C:N ratios of macroalgae were significantly lower in the BRC vs. FR
sites (15.8 vs. 21.0), in contrast to higher N:P ratios in the BRC (49.5 vs. 34.6), indicating
greater N-enrichment of the reefs within the Buccoo Reef itself. Overall, the 15N
contents of macroalgae averaged + 6.05 ± 1.59 o/oo and did not vary with season,
although the more remote and less populated sites off Little Tobago island did increase
significantly from the dry to wet season. However, the 15N contents of macroalgae in
the BRC (+ 6.62 o/oo) were significantly higher than the FR sites (+ 5.53 o/oo),
indicating a higher degree of wastewater derived N on the Buccoo Reef. The % cover of
coral correlated inversely with macroalgae among the reef sites, with the highest % cover
of macroalgae occurring throughout the Buccoo Reef Complex. These data suggest that
local inputs of sewage are a primary source of nutrient stress on Tobago’s reefs,
especially throughout the Buccoo Reef, and that improved collection and treatment of
wastewater could lead to improved water quality and reef health.
1. Introduction
Coral reefs are biologically diverse and economically valuable ecosystems that
provide an array of ecological services to coastal communities throughout their range.
Reef ecosystems occur in oligotrophic waters and are susceptible to eutrophication as a
result of low level nutrient pollution (Johannes, 1975; NRC 2000). Studies in Kaneohe
Bay, Hawaii, clearly showed how 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).
Pollution from land-based sources is now considered the single most important threat
to the marine environment of the Caribbean and impediment to sustainable use of its
resources (UNEP, 1994). Sources of nutrient pollution include sewage outfalls, septic
tanks, storm water runoff, fertilizers, deforestation (Likens, 2001; Lapointe and Thacker
2002) and atmospheric deposition (Barile and Lapointe, 2005).
The island of Tobago, often described as the “Jewel of the Caribbean”, is located at
the southern end of the Lesser Antilles off the coast of Venezuela. Tobago is primarily a
volcanic island but with considerable coral reef growth, especially in the southwestern
area where extensive coral reef development has resulted in a shallow limestone platform
known as the Buccoo Reef Complex (BRC; Fig. 1). The Buccoo Reef Complex
encompasses an area of ~ 7 km-2 and was officially designated as a marine protected area,
The Buccoo Reef Marine Park, in 1973 (Laydoo, 1991). The Buccoo Reef Maine Park is
the best example of contiguous coral reef – seagrass – mangrove ecosystem in the
Republic of Trinidad & Tobago. The BRC is also a major economic asset, attracting
some tens of thousands of visitors per year.
Like most marine protected areas in the Caribbean region, creation of the Buccoo
Reef Marine Park has not protected the area from water quality degradation. Many
coastal dwellings in the contiguous Buccoo Village area, for example, have septic tanks
and “soak-away” systems built in the carbonate-rich limestone that overlay the volcanic
geology. This sewage disposal technology provides little removal of nitrogen, which is
highly mobile in carbonate-rich systems and flows subsurface, via groundwater, into
coastal waters (Lapointe et al. 1990, Costa et al. 2000, Lapointe and Thacker 2001).
Similarly, secondarily treated sewage, a technology that does not remove nutrients
sufficiently to protect coral reef ecosystems, enters Buccoo Bay and the Bon Accord
Lagoon via several sewage treatment plants that service subdivisions near Buccoo
Village (Coral Garden Estates) and in Bon Accord. Sewage pollution in Buccoo Bay
presents a significant risk to public health as indicated by consistently elevated
concentrations of coliform bacteria and fecal streptococci (John 1996).
Although there has long been concern about sewage pollution in the Buccoo Reef
Complex, little is known about the dynamics by which nutrient pollution fosters
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 Buccoo Reef Marine Park (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 of the coral reef communities.
Like the Buccoo Reef Complex, fringing reefs around Tobago’s coast could also be
receiving increasing nutrient loads from poorly or inadequately treated sewage effluents.
Both large and small communities rely on “soak-aways” as on the BRC catchment or less
than adequate (i.e. tertiary level) treatment of waste water. Where centralized collection
and treatment systems for sewage have been developed they only provide only
secondary-level treatment at best (no nutrient removal) and are usually inadequate for the
end-volume, resulting in nutrient-rich discharges into rivers or wetlands that eventually
flow into coastal waters.
To specifically assess the chemical and ecological impacts of sewage pollution in the
Buccoo Reef Complex and the fringing reefs around Tobago, we undertook a water
quality sampling and coral reef monitoring project in 2001. The study involved
measurement of water column dissolved inorganic nitrogen (DIN), soluble reactive
phosphorus (SRP), and chlorophyll a during the dry (April - June) and wet (September –
October) seasons. This sampling design was necessary to address the seasonal effects of
the Orinoco River floodwaters that impact Tobago’s coastal waters during the wet season
(Laydoo, 1991). Underwater video of benthic reef communities was used to quantify
cover of hard corals, octocorals, macroalgae, turf algae, coralline algae, and sponges.
Stable nitrogen isotope ratios (15N) in benthic macroalgae were used to discriminate
among natural (N-fixation) versus anthropogenic (e.g. sewage) nitrogen sources fueling
algal blooms and eutrophication in the seasonal samplings.
2. Materials and methods
2.1 Study sites and sampling rationale - A total of six sites in the Buccoo Reef Complex
were sampled to assess water quality and benthic community structure along an inshore
to offshore gradient, to address the importance of land-based nutrient discharges. The
sites included a sewage outfall emptying into Buccoo Bay, a site immediately off the
shore in a location near the house where Prince Margaret honeymooned that we refer to
as Princess Reef and off Buccoo Point, near Buccoo Village, all in the inner BRC;
Walkabout Reef, where glass-bottom boat tour operators allow people to disembark and
walk on the backreef, and Nylon Pool, both in the middle of the BRC; and Coral Gardens
and Outer Reef in the offshore areas of the BRC (Fig. 1). We predicted that the inshore
sites of the Buccoo Reef Complex would show the strongest evidence of nutrient
enrichment from land-based runoff and that there would be a decreasing impact with
distance from shore. In addition, a variety of fringing reefs around Tobago’s Caribbean
and Atlantic coasts were sampled, which included a series of well known dive sites: Mt.
Irvine “Wall”, the Maverick (a sunken ship-artificial reef), Diver’s Dream, a site off shore
from 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. We hypothesized that nutrient enrichment would be relatively minimal off
Little Tobago Island, the site furthest offshore and flushed with oceanic “blue water”
waters of the Guyana Current and conversely, greater nutrient enrichment on the fringing
reef sites more directly impacted by land-based runoff from Scarborough and the more
urbanized areas of southwest Tobago, which includes sites off the Vanguard Hotel, Mt.
Irvine, the Maverick, Diver’s Dream and Diver’s Thirst. Finally, we sampled all sites in
both the dry and wet seasons of 2001 (Fig. 2) to assess the role of land-based storm water
runoff in driving seasonal shifts in nutrient concentrations and eutrophication.
2.2 Analysis of seawater for DIN, SRP, and chlorophyll a - SCUBA divers collected
water samples from the various reef sites between April 10 and June 20, 2001 in the dry
season and between September 24 and October 23, 2001 during the wet season. Water
temperatures and depths at the reef sites were measured using Oceanic Datamax Pro Plus
dive computers. Divers used clean, one liter polyethylene Nalgene bottles to collect
replicate (n = 4) seawater samples ~ 0.5 m off the bottom at the various reef sites. The
water samples were held on ice in the dark in a cooler until return to shore where aliquots
of the samples were filtered through a 0.45 m GF/F filter and frozen. The samples were
analyzed for DIN ( = NH4+plus NO3- plus NO2-) and SRP on a Bran and Luebbe
TRAACS Analytical Console at Harbor Branch Oceanographic Institution’s (HBOI)
Environmental Laboratory in Ft. Pierce, FL. The methods for collection, handling, and
processing of all nutrient samples followed a quality assurance/quality control protocol
developed by HBOI’s Environmental Lab. This plan prevented problems associated with
sample contamination and excessive holding times. Salinity of the water samples was
measured to ± 1.0 psu using a Bausch and Lomb refractometer. The GF/F glass fiber
filters used for filtering the water samples were frozen and analyzed for chlorophyll a
(chl a) as a measure of phytoplankton biomass. The filters were extracted for 30 minutes
using 10 ml of dimethyl sulfoxide and then with an added 15 ml of 90% acetone at 5 oC
overnight. The samples were measured fluorometrically before and after acidification for
determination of chlorophyll a and phaeopigment concentrations. Fluorescence
measurements were made using a Turner Designs 10-000R fluorometer equipped with a
infrared-sensitive photomultiplier and calibrated using pure chlorophyll a.
2.3 Analysis of macroalgae for C:N:P and 15N – SCUBA divers collected replicate (n =
2) composite samples of macroalgae from the various reef sites into nylon mesh bags. At
least 3-6 separate plants were collected for each composite sample of each species to
ensure representativeness.
Immediately following collection, the macroalgae were
cleaned of debris and transferred to plastic zip-loc baggies and held in a cooler during
transport to the lab. In the lab, the samples were identified, rinsed briefly (3-5 s) in
deionized water to further remove debris. The plants were placed in plastic drying dishes
and dried in a lab oven at 65 oC for 48 h. The dried macroalgae were ground to a fine
powder using a mortar and pestle and stored in plastic vials until analysis. Samples of
dried, powdered macroalgae were analyzed for stable nitrogen isotope ratios with a
Carlo-Erba N/A 1500 Elemental Analyzer and a VG Isomass mass spectrometer using
Dumas combustion (by Isotope Services, Los Alamos, New Mexico). The standard used
for stable nitrogen isotope analysis was N2 in air. 15N values, expressed as o/oo (ppm),
were calculated as [(Rsample/Rstandard) – 1] x 103, with R equal to 15N/14N.
Subsamples of the powdered macroalgae samples from the dry season sampling were
analyzed for C:N:P contents at Nutrient Analytical Services, Chesapeake Biological
Laboratory, University of Maryland System, 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 an IBM-compatible, Labtronics, Inc. DP500 software data
collection system (D’Elia et al. 1997).
2.4 Quantification of reef biota - 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 long belt transects at each reef site.
Divers obtained the imagery by holding the camcorder perpendicular to the reef surface
(0.5 m off bottom, 0.4 m-2 image area) and slowly swimming along the transects to obtain
clear, steady images. A second close-up oblique video transect was also recorded to
allow identification of algal taxa and to distinguish among the fine-scale (1-5 cm)
changes in biotic composition among these diverse and often multi-layered communities.
The digital video images were anaylzed on a high resolution color monitor using the
random point-count method. This method provided a relatively unbiased estimate of the
percent 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).
3. Results
3.1 Seawater DIN, SRP, and chl a
DIN concentrations measured during this study averaged 1.58 ± 1.08 (n = 107)
overall and varied both temporally (p < 0.0001) and spatially (p = 0.005) among the sites
(Fig. 3). The mean DIN concentration of all sites was lower (p < 0.0001) in the dry
season (0.66 ± 0.47 µM; n = 51) than the wet season (2.42 ± 0.73 µM; n = 56). The
seasonal increase in DIN was mostly the result of increased (p < 0.0001) ammonium
from the dry season (0.35 ± 0.20 µM; n = 51) to wet season (1.55 ± 0.57 µM; n = 56; Fig.
3). Nitrate also increased (p < 0.0001) from the dry season (0.31 ± 0.42 µM; n =51) to
the wet season (0.86 ± 0.51 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 of the BRC sites was higher (p = 0.012) than the
fringing reef sites in the dry season (0.86 ± 0.51 µM vs. 0.52 ± 0.39 µM) but not the wet
season (2.35 vs. 2.53 µM). The lowest mean concentrations of both DIN (1.04 ± 1.09)
and ammonium (0.66 ± 0.70) occurred at Black Jack Hole whereas the highest DIN (2.42
± 0.73 µM) and ammonium (1.95 ± 0.88 µM) occurred at Buccoo Point in the inner BRC.
SRP concentrations during the study averaged 0.23 ± 0.15 (n = 107) overall and
varied temporally (p = 0.034) and spatially (p < 0.0001; Fig. 4). The mean SRP
concentration of all sites was higher (p < 0.011) in the dry season (0.26 ± 012 µM; n =
51) than the wet season (0.20 ± 0.17 µM; n =56). Mean SRP concentrations of the BRC
sites were not significantly different than the fringing reefs sites either overall or in the
dry or wet seasons. The lowest SRP concentrations occurred at Black Jack Hole (0.18 ±
0.09 µM) and the highest at Buccoo Point (0.50 ± 0.61 µM), which was higher (p <
0.014) than all other sites.
The DIN:SRP ratios averaged 8.7 ± 6.5 (n = 51) during the study and varied both
temporally and spatially (Fig. 4). Overall, the mean DIN:SRP ratio was higher (p <
0.0001) in the wet season (13.9 ± 4.2; n = 56) than the dry season (2.9 ± 2.6; n = 51).
The DIN:SRP ratio was higher (p < 0.0001) in the BRC (4.0 ± 2.9; n = 20) than the
fringing reefs (2.3 ± 2.6; n = 31) in the dry season. However, in the wet season, the
DIN:SRP ratio was higher (p = 0.008) on the fringing reefs (14.6 ± 4.1; n = 44) than the
BRC (11.9 ± 3.7; n =26).
Chl a averaged 0.32 ± 0.19 µg/l at all stations throughout the study and varied
significantly temporally (p = 0.038) and spatially (p = 0.031; Fig. 5). 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. The lowest values in the dry season were at Coral Gardens (0.085 ± 0.02
µg/l) and the highest in the wet season were in the Bon Accord Lagoon (1.13 ± 0.16
µg/l). In the dry season, the mean chl a values were similar for the Buccoo Reef Complex
(0.23 ± 0.22 µg/l) and the Fringing Reefs (0.31 ±0.22 µg/l) whereas, in the wet season,
the mean chl a of the BRC (0.41 ± 0.24 µg/l) was greater (p = 0.031) than that of the FR
(0.32 ±0.10).
3.2 C:N:P and 15N in macroalgae
Macroalgae in the Buccoo Reef Complex were enriched in N but not P compared
to the fringing reef sites during the dry season (Table 1). The mean C:N (15.80 ± 5.78; n
= 16) for macroalgae in the BRC was lower (p = 0.014) than the Fringing Reefs (21.0 ±
6.58; n = 24) in contrast to the mean C:P values that were statistically similar (770 ± 294
vs. 759 ± 385).
These changes co-occurred with a higher (p = 0.002) N:P ratio in the
BRC (49.5 ± 15.6; n = 16) compared to the Fringing Reefs (34.6 ± 11.5; n = 24). The
lowest C:N ratio (8.0) occurred at Buccoo Point in the BRC and the highest (25.7) at
Black Jack Hole off Little Tobago Island. The lowest C:P (444) occurred at Buccoo
Point and the highest (1238) at Coral Gardens in the BRC. The lowest N:P (27.5)
occurred at Kelliston Drain off Little Tobago Island and the highest (61.6) at Coral
Gardens in the Buccoo Reef Complex.
15
The  N values of macroalgae averaged + 5.85 ± 1.23 o/oo (n = 174) throughout
the study and varied temporally, spatially, and by taxa (Fig. 6). The mean 15N value in
the dry season (+ 5.52 ± 1.24 o/oo; n=82) was lower (p = 0.01) than the wet season (+
6.14 ± 1.16 o/oo; n = 92). Overall, the mean 15N value of the fringing reef macroalgae
(+5.54 ± 1.29 o/oo; n=94) was lower (p < 0.0001) than that of the Buccoo Reef Complex
(+6.21 ± 1.06 o/oo; n = 80). The lowest 15N values in reef macroalgae occurred at
Black Jack Hole (+ 2.87 o/oo) and the highest at Princess Reef (+7.25 o/oo) in the inner
BRC. However, the highest 15N values (~ + 12 o/oo) of macroalgae were in nutrient
indicator chlorophytes (Ulva lactuca) and rhodophytes (Gracilaria tikvahiae, Agardhiella
subulata) collected adjacent to a wastewater outfall in Buccoo Bay (Fig. 6; Table 1).
When grouped by class, the 15N values varied significantly (p < 0.001) with the highest
values in rhodophytes (+7.0 ± 2.32 o/oo; n = 30), followed by chlorophytes (+ 6.23 ±
1.33 o/oo; n = 82) with the lowest in phaeophytes (+ 5.47 ± 1.23 o/oo; n = 54).
3.3 Quantification of reef biota
The reef sites in the inner BRC showed a distinct pattern of increased cover of
macroalgae and reduced coral cover (Fig. 7). The highest % cover of macroalgae (up to
40 %) occurred at Princess Reef and Buccoo Point where blooms of Halimeda opuntia,
Bryopsis spp., and Caulerpa spp. were observed (Fig 8 a,b,c). Coral cover was < 10 %
on these two sites compared to the more offshore sites (Coral Gardens, Outer Reef)
where coral cover ranging from 20 to 40 % was comprised of the genera Acropora,
Montastrea, Diploria, and Siderastrea (Figure 7). Algal turf was a major component of
these reef communities in the Buccoo Reef Complex with values ranging from up to ~ 50
% cover. The zoanthid Palythoa was another significant component of the BRC reef
communities and ranged up to > 20 % cover at Buccoo Point where it was observed
physically overgrowing the brain coral Diploria (Fig. 8d). The fringing reef sites had the
highest % hard coral cover (Culloden Reef, > 45 % cover), and generally lower frondose
macroalgae (< 10 % cover) but high cover of coralline algae (up to ~ 40 % cover; Figs. 7,
8d).
4. Discussion
Our water column nutrient data from Tobago are the first to document the role of
land-based nitrogen runoff in fueling varying degrees of eutrophication on the island’s
fringing coral reefs. Previous studies in Trinidad & Tobago have emphasized the role of
land-based 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 many coastal waters in the
Caribbean (Lapointe, 2004) and, combined with relatively low DIN:SRP ratios (<15:1),
suggest N rather than P limitation of algal growth (Lapointe et al., 1992). Such high
background SRP concentrations, low DIN:SRP ratios, and a tendency towards Nlimitation are indicative of a siliciclastic geology. This contrasts with the carbonate-rich
environments in Jamaica, the Bahamas, and the Florida Keys where low SRP
concentrations and high DIN:SRP ratios supports strong P-limitation (Lapointe et al.
1992). Hence, the natural volcanic geology of Tobago may predispose its coastal waters
for nitrogen rather than phosphorus limitation.
The differential effects of carbonate-rich vs. siliciclastic geology on N:P
availability in Tobago is apparent in both the Buccoo Reef Complex and the Fringing
Reef data in our study. Although the extensive limestone formation surrounding the
Buccoo Reef provides a sink for natural and anthropogenic SRP through adsorption onto
calcium carbonate surfaces (Berner, 1974; DeKanel and Morse, 1978), such is not the
case for DIN (Lapointe et al. 1990). This phenomenon explains how relatively high N:P
inputs from the Buccoo Reef watershed results in higher water column DIN:SRP and
macroalgal N:P ratios in the Buccoo Reef Complex compared to the Fringing Reef sites.
The elevated DIN:SRP ratios in the BRC were most pronounced during the wet season,
when wastewater loads from “soak-aways” and other sources in the watershed would be
maximal. Such high N:P inputs lead to P-limitation of primary production in carbonaterich 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” effects at the Fringing Reef sites outside of the Buccoo Reef
Complex results in lower DIN:SRP and N:P ratios, where N-limitation would be more
important.
Multiple lines of evidence from our study indicate that the reef at Buccoo Bay in
the Buccoo Reef Complex was the most nutrient impacted reef site in our study. The
highest DIN, ammonium, and SRP concentrations of the entire study occurred at Buccoo
Point, a reef directly impacted by wastewater discharges from the adjacent upland
watershed. The lowest C:N and C:P ratios of all macroalgae in the study also occurred at
Buccoo Point, demonstrating impacts of these 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). These researchers
found higher fractions of organic P in the coral cores in the BRC than Culloden reef, and
that temporal patterns in both total and organic P in the BRC coral cores correlated with
human activities on the watershed. Our results also support previous findings by the IMA
(1996) that the highest nutrient concentrations in southwest Tobago occurred in Buccoo
Bay and the Bon Accord Lagoon, both of which have received increased wastewater
nutrient loadings in recent decades.
The effects of high nutrient concentrations with high DIN:SRP ratios in the BRC
were evident in the increased biomass and C:N:P contents of macroalgae in the BRC
compared to the FR.
Macroalgae in the BRC were enriched in N compared to the FR
sites, resulting in a lower C:N (15 vs. 21) and higher N:P (50 vs. 35) ratio. The lower
C:N ratio reflects reduced N-limitation of growth, and explains the overall higher
macroalgal biomass in the BRC compared to the FR sites. The relatively high N
enrichment in the BRC drives the macroalgae to increased P-limitation, evidenced by the
higher N:P ratio of macroalgae in the BRC compared to FR. Blooms of the chlorophytes
Bryopsis, Caulerpa, and Halimeda were observed overgrowing reef biota and
frameworks in the BRC, a phenomenon that was not observed at any of the FR sites. The
phenomenon by which high N:P inputs from the watershed drive macroalgal blooms 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), Martinique (Littler et al. 1992), and Bermuda (Lapointe
and O’Connell, 1989).
The identification of wastewater as the source of elevated DIN in the BRC was
apparent from the elevated 15N values of macroalgae in the BRC compared to the FR
sites.
Numerous studies have shown how 15N values in macroalgae faithfully
discriminate among various natural and anthropogenic nitrogen sources (see Risk et al.
2009 for a review). For example, France et 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 o/oo, a value close to the atmospheric signature of 0 o/oo and indicative of nitrogen
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), southwest Florida (Lapointe and Bedford, 2007), Florida Keys (Lapointe et al.
2004), and Moreton Bay, Australia (Costanzo et al. 2001) all reported 15N values
ranging from ~ + 3.0 – + 15 o/oo, with higher values > 8 o/oo in close proximity to the
wastewater source. This pattern was consistent with our results where the highest 15N
values of ~ + 12 o/oo were in “nutrient indicator species” (Ulva lactuca, Gracilaria
tikvahiae, Agardhiella subulata) near a wastewater outfall in Buccoo Bay; the lower
mean value of + 7.25 o/oo for Princess Reef in inner Buccoo Bay and + 6.21 o/oo for
macroalgae throughout the BRC would be expected from increasing dilution of landbased wastewater N throughout the BRC. These 15N data support the hypothesis that
the entirety of the BRC has been significantly impacted by DIN derived from
wastewaters via submarine groundwater discharge of leachate from “soak-aways” or
direct discharges from sewage outfalls. 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 values of + 2.5 o/oo for macroalgae at
Black Jack Hole off Little Tobago Island in the dry season were indicative of more
oligotrophic and “natural” nitrogen sources, although these values increased significantly
during the wet season as a result of more widespread dispersion of land-based sewage
pollution via stormwater runoff.
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 decreased DIN concentrations, but not SRP. This pattern results from rapid uptake
of DIN -- the primary limiting nutrient-- by phytoplankton in coastal waters receiving
land-based sewage pollution. These findings support previous observations in Kaneohe
Bay, Hawaii (Laws and Redalje 1979) and the Florida Keys (Lapointe and Clark 1992)
that chl-a provides 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, such as those we observed on reef sites in the inner
BRC. Classic “indicator species” of nutrient enrichment, including the macroalgae Ulva,
Halimeda, Bryopsis, Caulerpa, and Sargassum were abundant on reefs in the BRC that
had DIN concentrations > 0.5 M. In contrast, macroalgae were less abundant on the
fringing reefs around Tobago that had lower DIN concentrations.
The loss of hard coral cover and 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 loss of hard corals and
macroalgal blooms have occurred over the past two decades in the BRC, a MPA with
abundant 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) but also dense populations of reef 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
may have increased grazer populations (both echinoids and herbivorous fishes) in the
BRC where growth is typically limited by dietary nitrogen (Lapointe, 1999). Reef health,
biodiversity and the ecological services have been reduced by sewage-driven
eutrophication in the BRC despite abundant populations of grazers.
In summary, our results support the conclusion of Siung-Chang (1997) for the
Caribbean region and Agard and 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. Ray DeBeer and the World of
Watersports for providing dive boat support that made this research possible. This
research was supported by the Buccoo Reef Trust and the Harbor Branch Oceanographic
Institution, Inc. This is contribution number
from the Harbor Branch Oceanographic
Institute at Florida Atlantic University, Ft. Pierce, FL.
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Figure 1. Map of Tobago showing locations of monitoring sites in the Buccoo Reef
Complex and fringing reefs.
Figure 2. Cumulative monthly rainfall measured at Crown Point, Tobago, during 2001.
Figure 3. Concentrations of ammonium, nitrate, DIN, and the f-Ratio for monitoring sites
in the Buccoo Reef Complex (left side) and fringing reefs (right side) in the dry (April –
June) and wet (September – October) seasons, 2001. Values represent means ± 1 SD (n =
4).
Figure 4. Concentrations of soluble reactive phophorus (SRP and the DIN:SRP ratio for
monitoring sites in the Buccoo Reef Complex (left side) and fringing reefs (right side) in
the dry (April – June) and wet (September – October) seasons, 2001. Values represent
means ± 1 SD (n = 4).
Apr-Jun
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Figure 5. Concentrations of chlorophyll a for monitoring sites in the Buccoo Reef
Complex (left side) and fringing reefs (right side) in the dry (April – June) and wet
(September – October) seasons, 2001. Values represent means ± 1 SD (n = 4).
Figure 6. 15N values of macroalgae at monitoring sites in the Buccoo Reef Complex
(left side) and fringing reefs (right side) in the dry (April) and wet (September – October)
seasons, 2001. Values represent means ± 1 SD (n = 4).
Figure 7. Percent cover of reef biota at reef sites in the Buccoo Reef Complex (Princess
Reef, Buccoo Point, Coral Gardens, Buccoo Reef) and fringing reefs (Arnos vale,
Culloden, Englishman’s Bay, and Three Sister’s). Values represent means ± 1 SD (n=4).
Figure 8. Photos of reef biota (a,b,c,d).
Table 1. Tissue C:N:P contents of macroalgae from reef sites in the Buccoo Reef
Complex (BRC) and fringing reefs around Tobago.
LANGTON paragraphs for discussion??
Macroalgal overgrowth on coral reefs clearly reflects a well documented phase shift
resulting in the demise of the reef itself (references??), which raises the question as to the
cause and potential controls behind such shifts. In the current study we found, in general
terms, a nutrient gradient from inshore to offshore and/or from the least populated end of
the island, in the northeast, to the most highly populated southwest Tobago. It is clear
that human activity is impacting the near shore coral reefs and land-based nutrients are
fueling a shift from coral to macroalgae. The solution is to remove the nutrients prior to
wastewater discharge into the sea, and although that is technologically possible and
under considered, the more urgent question is whether or not there is an ecological
mechanism to control the proliferation of macroalgae while the existing methods of waste
water treatment are our only option.
In the case of Tobago, as virtually all of the Caribbean, the major invertebrate macroalgal
predator, Diadema antillarum was lost several decades ago and continues to be slow to
recover (Frey, 2004). Vertebrate herbivores include a number of fish species and variety
of feeding guilds, but studies on fish feeding (eg. McClanahan et al., 2000; Ledlie et al
2007) have documented the avoidance of macroalgae as a food choice by many of the
more common herbivorous reef fish. This begs the question as to how to slow or reverse
a phase shift to favor coral recovery. Mumby et al. (2006) found a negative correlation
between grazing by parrot fish and macroalgal cover, but this is somewhat
counterintuitive considering that macroaglae is not a preferred prey item by most
herbivorous fish (Ledlie et al 2007). Presumably, what is happening is that as the
intensity of grazing by parrot fish on epilithic algae within the confines of a Marine
Protected Area increases, due to a complex predator/prey relationship, this substrate
disturbance reduces the settlement and growth of macroalgae, as has been reported by
Lewis, 1986; Williams et al. 2001 and Paddack et al. 2006. Although fish are often
opportunistic feeders, and there is a well documented case, of what was termed the
identification of a “sleeping functional group” (Bellwood et al. 2006) where an
invertebrate and plankton feeding batfish shifted its diet to consume macroalgae, there is
little evidence to suggest that this mechanism offers a universal solution to the problem of
nutrient overload on coral reefs. Despite a relatively healthy and abundant herbivorous
fish population, as found in the Buccoo Reef complex (Frey, 2004), we still find the
proliferation of macroalgae reflecting an overload of land-based nutrients and no really
viable mechanism for reversing this trend.