Marine Pollution Bulletin 60 (2010) 1018–1030

Contents lists available at ScienceDirect

Marine Pollution Bulletin

journal homepage: www.elsevier.com/locate/marpolbul

Historical analysis (2000–2005) of the coastal water quality in San Andrés Island,
SeaFlower Biosphere Reserve, Caribbean Colombia
Brigitte Gavio a,b,*, Shelly Palmer-Cantillo a,c, J. Ernesto Mancera a,b
a
Universidad Nacional de Colombia, Sede Caribe, San Luis Free Town, 52-44 San Andrés Isla, Colombia
b
Departamento de Biología, Universidad Nacional de Colombia, Sede Bogotá, Ciudad Universitaria, Edificio, 421 Bogotá, D.C., Colombia
c
Corporación para el Desarrollo Sostenible del Archipiélago de San Andrés, Providencia y Santa Catalina (CORALINA), Vía a San Luis Bight Km, 26 San Andrés Isla, Colombia

a r t i c l e i n f o a b s t r a c t

Keywords: To understand the coastal water quality of San Andrès Island, and provide tools for the management of its
Coastal water monitoring marine resources, we present the historical analysis of the island monitoring, which includes ammonia,
Pollution nitrites, nitrate, phosphates, fecal and total coliforms. The anthropogenic pressure on the coastal system
Nutrification is heavy, with water nutrification, posing at risk seagrass and coral ecosystems. During dry season, bio-
Insular Caribbean Colombia
logically available nitrogen is 3–9 times higher than the maximum recommended for coral reefs, while
Coliforms
during wet season values are 2–6.4 times the maximum. Biologically available phosphorous is also high,
1–8 times the maximum during dry season, 2–13 times during wet season. In some sites the concentra-
tion of pathogenic bacteria is above the limits set by law for primary and secondary contact. It is urgent to
improve the management of sewage discharge, the main polluting source of San Andres coastal waters.
Ó 2010 Elsevier Ltd. All rights reserved.

1. Introduction 290 km off the coast of Nicaragua and 480 km off the coast of
Cartagena (Colombia).
The Caribbean is the world’s region most dependent of tourism The island has an area of 25 km2; with a resident population of
(Kingsbury, 2005), with the typical attraction of ‘‘sun, sand and 55.426 habitants (DANE, 2005), equivalent to 2217.04 habitants/
sea”, where visitors are attracted by the pristine conditions of its km2, it is maybe the most densely populated island of the Carib-
coasts. Therefore, marine pollution problems are particularly men- bean (Diaz et al., 1996). In 2001 the whole archipelago was de-
acing in this area. The Caribbean coastal area has not reached, yet, clared by UNESCO a Biosphere Reserve, under the supervision of
pollution levels seen in other regions (Harborne et al., 2001). How- the Corporation for the Sustainable Development of San Andrés,
ever, in the last 20–30 years, marine pollution and coastal degrada- Old Providence and Santa Catalina Archipelago, CORALINA.
tion have become serious issues (Siung-Chang, 1997). The island’s major incomes are tourism and commerce, fol-
As previous studies have revealed, the main polluting problems lowed by fishery. San Andrés fits well as a typical Caribbean insular
of the coastal waters in the Caribbean are oil spills and untreated country: it is highly dependent on tourism, its population in-
sewage pollution, followed by solid wastes (mainly domestic), creased with little or no land planification, leading to a chaotic
industrial pollution and pesticides (Siung-Chang, 1997; Debrot coastal development, the sewage system covers only 8% of the res-
et al., 1999; Mignucci-Giannoni, 1999; Harborne et al., 2001; Boc- ident population (SIGAM/CORALINA, 2004), without any treatment
quené and Franco, 2005). These problems are emphasized by the prior to its disposal into the ocean.
fact that the Caribbean Sea is a closed basin with little water ex- The great majority of the population wastewater is disposed in
change (Atwood, 1977, cited in Panke and Quimby, 2000), making septic tanks, but its leaking has polluted not only great part of the
it an ideal place for the accumulation of pollutants (Panke and Qui- drinking water wells of the island, is also impacting heavily its
mby, 2000). nearshore waters and ecosystems (Marín and Cadavid, 2001).
San Andrés Island is part of the San Andrés, Old Providence and It has been estimated that a total of 14.466 m3 of untreated
Santa Catalina Archipelago, and lays in the Caribbean region, sewage water is discharged daily in the coastal waters of the island
(data for 2000, Steer et al., 1997), which means, approximately, a
discharge of 1.91 ton/day of SST, 3.23 ton/day of DBO5, 1.45 ton/day
of oils and lubricants, 0.7 ton/day of nutrients and about 1.49 
* Corresponding author. Address: Departamento de Biología, Universidad Nac-
1018 NMP/day of fecal coliforms (INVEMAR, 2002).
ional de Colombia, Sede Bogotá, Ciudad Universitaria, Edificio, 421 Bogotá, D.C.,
Colombia. Tel.: +57 8 5133310; fax: +57 8 5133310x15. Other polluting fonts are the inadequate solid waste disposal, in
E-mail address: [email protected] (B. Gavio). a ‘‘basurero” (open-air garbage dump), whose lixiviates reach the

0025-326X/$ - see front matter Ó 2010 Elsevier Ltd. All rights reserved.
doi:10.1016/j.marpolbul.2010.01.025
 B. Gavio et al. / Marine Pollution Bulletin 60 (2010) 1018–1030 1019

coast, illegal oil spill from boats, and deterioration of mangrove vide better tools for the environmental management of its marine
ecosystems (Marín, 2001; INVEMAR, 2001). The overexploitation resources.
of the marine resource is another important concern in the island,
and is severely putting at risk the coral reefs nearby (Burke and 2. Materials and methods
Maidens, 2005).
CORALINA, the highest environmental authority of the Archipel- 2.1. Study site
ago, started a water quality monitoring program of the coastal
water of the island in 1997. There are no formal studies prior to San Andrès is a small island (25 km2) (Fig. 1) that lies between
the monitoring program on the coastal water quality of the island, 12°280 5800 and 12°350 5500 N and 81°40’4900 and 81°430 2300 W (IGAC,
being the monitoring program run by CORALINA part of REDCAM, 1986). It forms part of the Archipelago of San Andrès, Providencia
(Red de vigilancia para la conservación y protección de las aguas and Santa Catalina, and it is the administrative center of the
marinas y costeras de Colombia), directed by INVEMAR (Instituto Department, and the main touristic target. The population is con-
de Investigaciones Marinas y Costeras ‘‘José Benito Vives de And- centrated in the northern part of the island (around 7000 habi-
réis”). This lack of previous data, extended to the entire country, tants/km2), as well as the tourism. Towards the center and the
is due partially to a historical lack of interest of Colombia to its south, the population density is much lower and the island still
sea and its resources (Steer et al., 1997; INVEMAR, 2001). Only in maintains rural characteristics.
1993, the environmental authorities in the country (the Ministry The island, and the rest of the archipelago, is volcanic in origin.
of Environment and the Regional Autonomous Corporations for The subsidence of the volcanic base, and its simultaneous cover
Sustainable Development) were created, and few years later with calcareous deposits, biogenic in origin, during the Tertiary
(2000) the Environmental Politic for Coastal Zones was finally and Quaternary, gave rise to the present island (Diaz et al., 1996).
established (INVEMAR, 2001). The marine platform on the oriental side is shallow, and gets to
The objective of the present paper is to provide the first analysis the coral reefs in the open ocean, which mitigate the waves. On this
of the monitoring data of CORALINA, in the time span 2000–2005. submarine terrace there are deposits of corals, coralline algae,
We hope the present work will help to better understand the cur- urchins and other animals, which produce calcareous sand
rent situation of the coastal waters of San Andrès Island, and pro- (Geister, 1975).

Fig. 1. The island of San Andrés in the Caribbean Sea showing sample site location.
1020 B. Gavio et al. / Marine Pollution Bulletin 60 (2010) 1018–1030

On the west side of the island, the transition is much more Along the northeast coast of the island the currents are slow,
abrupt, with cliffs indicating strong marine erosion (IGAC, 1986). with the maximum speed (10 m/min) close to the reef. In the pro-
The island lies in the transition zone between tropical dry and tected areas the current velocity does not exceed 4–5 m/min, with
tropical wet climate. The influence of trade winds mitigates the the same wind conditions (Garay and Castro, 1993).
dry and warm climate. The annual mean temperature is 27.4 °C, The archipelago is influenced by the Caribbean current which
with maximum values between 29 and 30 °C (May–June) and min- originates temporal convergent whirlpools affecting the distribu-
imum between 25.5 and 26.0 °C (December–February). The annual tion and concentration of plankton and associated nutrients (Garay
mean precipitation is 1797.8 mm, unevenly distributed in a dry et al., 1988).
season (January–April), with stronger winds, and a wet season
(October–December) when 80% of the annual rain falls. During
the period May–July the rains are moderate in intensity (IDEAM, 2.2. Monitoring protocol
1995).
The predominant currents around San Andres Island are caused CORALINA, the corporation responsible of monitoring the coast-
by the north-east trade winds (Díaz et al., 1995). Currents intercept al water quality of the Archipelago, started the monitoring pro-
the island from the northeast, running through the barrier reef and gram in 1997, as part of the program REDCAM of the INVEMAR.
diverging to the south of the island. Current velocity is reduced by They sample twice a year, once during the dry season (January–
the barrier reef and becomes weaker on the western coast of the May), and once during the wet season (June–December), in 14 sites
island (Díaz et al., 1995). Waves formed in the open sea break di- around the island (Fig. 1), 60 m off the coast, at a water depth of
rectly on to the barrier reef, and diffract around the island. 30 cm.

Fig. 2. Nitrate concentration (lg/L). A–C dry season. D–F wet season.
 B. Gavio et al. / Marine Pollution Bulletin 60 (2010) 1018–1030 1021

Fig. 2 (continued)

The sites Punta Hansa, Hotel Isleño and Punta Norte are located discharges were, and still are, directly released in the bay. In
in northern portion of the island, in front of the most populated 1996, the harbor was built north to the bay, and the communica-
beaches and the center of the town. Cabañas Altamar is in front tion of the bay with the open water was reduced to a shallow
of a district less populated than the center, on the western side and narrow channel, reducing even more its hydrodynamics and
of the island. Alcantarillado is where the sewage system gets to consequent water exchange. The bay is surrounded by a mangrove
the sea, however, since September 2007 there is a submarine sys- wetland, which has been declared regional park (Mangrove Regio-
tem which brings the wastewater offshore, on the western side of nal Park Old Point) by CORALINA in 2002, together with the bays.
the island. El Cove is a small closed bay, once a harbor for the army; In Bahía Hooker CORALINA has two sampling sites, one inside
Yellow Moon and Rocky Cay are sites in front of two hotels on the the bay, where mangroves are, and one where the electric plant
eastern coast, but the area here is much less populated than the once was. Muelle is the harbor of the island, where large boats ar-
north. Bahía Hooker is an enclosed bay, which in the past has been rive daily to bring the comestible goods and other merchandise to
under heavy anthropogenic pressure (Lonin and Mendoza, 1997). the island (almost all the goods are imported from mainland).
In 1961, an electric plant was installed here, and the water used Johnny Cay is a small rocky islet, in front of the northern part of
to refrigerate the plant was directly discharged in the bay, together the island, where tourists go to spend the day. The islet is not per-
with oil and combustible of the same plant. In 1974, a district of manently inhabitated, but few restaurants are active daily to re-
approximately 75 houses was built close by, and all the sewage ceive the tourists. Influencia Basurero is on the west coast of the
1022 B. Gavio et al. / Marine Pollution Bulletin 60 (2010) 1018–1030

island, and is the site where running off from the solid garbage dis- perature, salinity, pH, etc.). However, the present paper focuses
posal system of the island gets to the ocean. Finally, Frente Sharky’s exclusively on the nutrient and coliform analysis, which was
is also on the west coast of the island, where few houses are started in 2000.
inhabitated.
In each site, they collect water samples to determine nitrites, ni- 3. Results
trates, ammonia, phosphates, fecal coliforms and total coliforms.
The water samples were collected in plastic bottles (500 ml) 3.1. Nitrites
and transported (refrigerated to 4 °C) to the laboratory. For nutri-
ent analysis, they follow APHA protocols (APHA, 1995; Garay Nitrites concentration was below the minimum detectable
et al., 2001). The analyses were run on a spectrophotometer Spec- (2 lg/L) most of the time at all sites (data not shown). Only in
tronic 5 Genesys, with a minimum detection range of 2 lg/L. Alcantarillado, Hooker Bay (both sites) and Influencia Basurero
To determine the number of coliforms, they used the method of the registered values are above the minimum detectable for some
colony formation (membrane filtering) until 2000. In 2001, they years. In Alcantarillado, concentrations of 3 lg/L were detected for
changed to the more probable number (both techniques described the dry season of 2001 and 2002, 5 lg/L in the dry season of 2004
in Garay et al., 2001). They also measure other parameters, (tem- and 2 lg/L for both seasons of 2005. In Hooker Bay (Mangrove)

Fig. 3. Ammonia concentration (lg/L). A–C dry season. D–F wet season.
 B. Gavio et al. / Marine Pollution Bulletin 60 (2010) 1018–1030 1023

Fig. 3 (continued)

Table 1
N:P ratio. 3 lg/L were detected for the dry seasons of 2001 and 2003. In Hoo-
Estación Dry season Wet season ker Bay (plant) 6 and 5 lg/L were registered in the dry season of
2001 and 2003, respectively. In Influencia Basurero, 3 lg/L were re-
Punta Hansa 4.8 3.3
Hotel Isleño 3.7 3.0 corded in the dry season of 2001.
Punta Norte 4.2 3.1
Cabañas Altamar 16.9 5.9
Alcantarillado 4.8 3.9 3.2. Nitrates
El Cove 7.8 2.9
Yellow Moon 5.2 2.7 For the nitrate concentration, values are generally higher during
Rocky Cay 2.3 5.0
Bahía Hooker (manglar) 13.7 1.5
dry season (Fig. 2a–c) than during wet season (Fig. 2d–f), with the
Bahía Hooker (plantas) 7.4 1.4 exception of the years 2004 and 2005, when nitrate values are
Muelle San Andrés 13.3 3.5 higher during rainy season.
Jhonny Cay 9.5 1.8 Most stations show a similar behavior for nitrate concentra-
Influencia Basurero 58.5 6.4
tions, where most stations show comparable values across the
Frente Sharky’s 4.5 1.6
years sampled. The nitrate concentration value range from <10 to
1024 B. Gavio et al. / Marine Pollution Bulletin 60 (2010) 1018–1030

540 lg/L (Fig. 2). During dry season, in the year 2001 Influencia and 2004, at all sites the ammonia concentration were below
Basurero showed an anomalous concentration of 524 lg/L 10 lg/L; only Alcantarillado recorded 14 lg/L in 2004.
(Fig. 2a) while the other years sampled, in the dry season, values During wet season, ammonia values are generally higher, and
were always below 100 lg/L. In 2000, during the wet season, the range between 13 and 95 lg/L (Fig. 3d–f). In Punta Hansa, Isleño,
highest values of nitrate were recorded for most sites (Fig. 2d Punta Norte and Rocky Cay, no data were taken in 2000 (Fig. 3f).
and f) with the exception of Yellow Moon (Fig. 2e), Jhonny Cay As in the dry season, in 2001 abnormal values were detected in
and the Cove (Fig. 2f). Alcantarillado (140 lg/L) and Influencia Basurero (15,480 lg/L)
(Fig. 3d), while in 2004 Alcantarillado had an ammonia concentra-
tion of 136 lg/L. During the wet season of 2002, values at all sites
3.3. Ammonia were below 10 lg/L, while the following year ammonia concentra-
tions were high everywhere, ranging between 47 and 69 lg/L. In
Ammonia concentration are generally lower in dry season general terms, ammonia concentration is considerably higher dur-
(Fig. 3a–c) than during wet season (Fig. 3d–f). During dry season, ing wet season, than during dry season (Fig 3).
values normally range between <10 and 75 lg/L. During 2000, in
Yellow Moon a high value of 197 lg/L was detected (Fig. 3c) while 3.4. Phosphates
in 2001 anomalous values of 137 and 1900 lg/L were registered for
Alcantarillado and Influencia Basurero, respectively. In 2002, During dry season, phosphate concentration generally range be-
Alcantarillado had a value of 405.6 lg/L (Fig. 3a). During 2003 tween 8 and 60 lg/L (Fig. 4a–c), with anomalous values of 179 and

Fig. 4. Phosphate concentration (lg/L). A–C dry season. D–F wet season.
 B. Gavio et al. / Marine Pollution Bulletin 60 (2010) 1018–1030 1025

Fig. 4 (continued)

170 lg/L at Alcantarillado, for 2004 and 2005 (Fig. 4a). During wet the N:P is even lower, ranging from 1.4 (Hooker Bay, plant) to
season, phosphate values are generally higher, ranging from 8 to 6.4 (Influencia Basurero) (Table 1).
121 lg/L (Fig. 4d–f). In 2001, Influencia Basurero showed a peak
value of 2445 lg/L. Compared to the other years, the wet season 3.6. Fecal coliforms
of 2003 showed higher values of phosphates at all sites.
Only since 2001, the counting of coliforms (fecal and total) are
expressed as more probable number (MPN)/100 mL. From 1997
3.5. N:P ratio to 2000, they were estimated as colony-forming units (CFU). There-
fore, we only present the data from 2001 to 2005, since the two
During the dry season, the relationship N:P is generally low, methods are not comparable. Hotel Isleño presents counting of
ranging from 2.3 (Rocky Cay) to 16.9 (Cabañas Altamar), evidenc- 210 NMP/100 mL during both seasons of 2001 (Table 2). In Punta
ing that the primary productivity is limited by nitrogen in these Norte 11,000 NMP/100 ML were detected in the rainy season of
waters. Only Influencia Basurero has a relationship N:P of 58.5, 2001. Alcantarillado has high values during most of the sampling,
indicating that P is the limiting factor. During the rainy season, El Cove has high number of coliform during the dry season of
1026 B. Gavio et al. / Marine Pollution Bulletin 60 (2010) 1018–1030

2001 (16,000 NMP) and 2003 (300). In Yellow Moon 11,000 NMP/ year with the exception the rainy season of 2003 and 2005; Hooker
100 mL were detected in the rainy season of 2001, Hooker Bay Bay (mangrove) where counting were always above the limits,
(mangrove) revealed high numbers in 2001 (both seasons) 2003 with the exception of 2003 (rainy season) 2004 (dry season) and
dry season and 2004 rainy season. The other site in Hooker Bay 2005 (dry season); and Hooker Bay (plant) where the limits were
(plant) had high concentrations of fecal coliforms (ranging not passed only in 2002 (rainy season) 2003 (rainy season) 2004
from 210 to >16,000 NMP/100 mL) during the whole time log (dry season) and 2005 (rainy season). As for the fecal coliforms,
examined, with the only exception of the rainy season of 2002, during the dry season there is a major concentration of total coli-
when 60 NMP/100 mL were detected. forms than during the rainy season.
In Johnny Cay during the dry season of 2001 there were 330
NMP/100 mL, while in the rainy season 200 NMP/100 mL were de-
tected. In the other years the counting was low. Generally the fecal 4. Discussion
coliform counting is higher during the dry season. In Colombia, the
decreto 1594 of 1984 determines the maximum limits of fecal and 4.1. Nutrients
total contaminants in coastal waters for recreational use. For fecal
contamination, the maximum limit for primary contact is 200 Several recent reviews found that tropical marine ecosystems
NMP/100 mL, while there is no limit assigned for secondary do not fit the established eutrophication paradigm currently ap-
contact. plied to management decisions (Bianchi et al., 1999; Pennock
et al., 1999). Few models, mass budgets, and synoptic measures
3.7. Total coliforms of processes are known for tropical polluted marine ecosystems
(Dudgeon, 1992). The amounts of solar, mechanical (wind, tides
According to the law (Decreto 1594 of 1984, Ministerio de Pro- and waves), and chemical energies together with regional geomor-
tección Social, 1984), the maximum limits for total coliform in rec- phology, establish the template from which site-specific patterns
reational waters are the following: 1000 NMP/100 mL for primary of primary productivity develop for marine ecosystems (Odum
contact and 5000 NMP/100 ML for secondary contact. These limits et al., 1972). Light availability, residence time and nutrient inputs,
are passed by several sites particularly in 2001 (both seasons), which are controlled by the geomorphology and geophysical pro-
2003 (dry season) and 2004 (rainy season) (Table 3). The sites most cesses, are three key factors limiting primary productivity among
contaminated are Alcantarillado, where limits were passed every the geomorphological types (Cloern, 1999). Reef environments,

Table 2
Fecal coliforms (NMP/100 mL) during dry and wet seasons.

Site 2001 2002 2003 2004 2005

Dry Wet Dry Wet Dry Wet Dry Wet Dry Wet
Punta Hansa 90 90 40 <2 <2 13 <2 <2 <2
Hotel Isleño 210* 210* 60 <2 <2 2 <2 <2 <2
Punta Norte 60 11,000* 40 <2 <2 <2 <2 <2 <2
Cabañas Altamar 70 90 90 <2 80 <2 <2 <2 2
Alcantarillado 16,000* 11,000* 90 >16,000* 20 >1600* <2 >1600* <2
El Cove 16,000* 150 70 300* 90 110 170 13 4
Yellow Moon 11,000* <20 <20 <2 <2
Rocky Cay <20 110 60 70 80 <2 80 <2 <2
Bahía Hooker (manglar) 800* 1200* 90 >16,000* 40 <2 500* 4 7
Bahía Hooker (plantas) 210* 11,000* 60 >16,000* 300* 300* 900* 500* 240
Muelle San Andrés 140 110 20 90 20 22 70 22 7
Jhonny Cay 330* 200 <20 <20 <20 <2 <2 <2 <2
Influencia Basurero <20 <20 <2 <2 <2 2
Frente Sharky’s <20 <20 <2 <2 <2

Values marked with  are above 200 (NMP/100 mL), the limits for primary contact set by Law (Decreto 1594 of 1984). For secondary contact no limits are set.

Table 3
Total coliforms (NMP/100 mL) during dry and wet seasons.

Site 2001 2002 2003 2004 2005

Dry Wet Dry Wet Dry Wet Dry Wet Dry Wet
Punta Hansa 90 90 140 20 20 22 80 2 2
Hotel Isleño 260 210 90 20 20 17 8 2 13
Punta Norte 170 11,000** 170 20 20 4 2 4 4
Cabañas Altamar 1700* 90 170 230 1100* 2 50 11 6
Alcantarillado 16,000** 11,000** 1300* 16,000** 800 1600* 1600* 1600* 2
El Cove 16,000** 150 210 300 9000** 300 300 27 4
Yellow Moon 11,000** 20 20 N.A 2 4
Rocky Cay 170 110 110 110 230 2 300 4 2
Bahía Hooker (manglar) 3500* 1200* 16,000** 16,000** 800 7 1600* 34 1600*
Bahía Hooker (plantas) 16,000** 11,000** 80 16,000** 800 900 1600* 1600* 900
Muelle San Andrés 16,000** 11,000** 70 2400* 210 240 1600* 130 9
Jhonny Cay 16,000** 2100* 20 20 20 2 2 2 2
Influencia Basurero 150 20 7 2 2 2
Frente Sharky’s 20 20 2 2 2

Values with  are above the limits set by Law (Decreto 1594 of 1984) for primary contact (1000 NMP/100 mL); the  values are above the limits for secondary contact (5000
NMP/100 mL).
 B. Gavio et al. / Marine Pollution Bulletin 60 (2010) 1018–1030 1027

with low nutrients and long water residence time, have very clear gal blooms (Heisler et al., 2008), with all its consequences. Dis-
waters and low wave energies that support productive seagrass solved nutrient concentrations are usually much lower in tropical
and coral communities, but low phytoplankton production. In surface waters than in temperate waters. An increase of phospho-
addition, these environments usually have a limited intertidal wet- rus concentrations by 0.75 lM in an estuary along the Atlantic
land: water surface area ratio. The response of each type of primary coast of North America may increase the concentration 2-fold.
producer to nutrient enrichment will determine the susceptibility Yet that same concentration increase in a tropical estuary, say in
to eutrophication in each coastal setting. the Caribbean Sea, would be approximately a 40-fold increase.
Suspended load and light are two important factors related to The implications of this for tropical community structure and func-
the response of marine systems to nutrient over-enrichment tion are not clear, but the possibility exists that the impact of a gi-
(Cloern, 1999). Light levels can play a critical role in response of ven increase in nutrient concentrations on a nutrient-poor tropical
systems to nutrient loading, and there is certainly high incident marine community might be much greater than that on a typical
light year round in tropical latitudes. During peak discharge, total temperate marine community (Hatcher et al., 1989).
suspended solid concentrations are high in the coastal zone, but Nutrient enrichment will enhance net primary productivity par-
are lower in dry season. These differences in water clarity between ticularly in those environmental settings with high light and longer
wet and dry season are important in regulating patterns of primary residence time of water, such as marine-dominated embayments.
productivity. Nutrient loadings that include a decrease in N:P ratios will
Residence time of water in coastal zone is an important factor disproportionately increase productivity in carbonate systems as
relating loading rates to ecological processes. High tidal energy phosphorus becomes more available. Reef and lagoons are
prevents the development of eutrophication in spite of sewage marine-dominated embayments with clear waters that have a long
waste from urban watersheds. Thus, the relatively rapid water re- residence time; yet these waters are oligotrophic usually with
newal (11.4 days for the renewal of 50% of the bay water volume) higher N:P ratios. These are sites of high seagrass distribution
explains why Baia de Guanabara in Brazil has reasonable water and productivity, with limited phytoplankton production and
quality in the lower parts of the bay where huge quantities of un- reduced inputs from mangrove wetlands. Tropical habitats in
treated sewage are discharged (Kjerfve et al., 2001a, b). In the Gua- marine-dominated embayments, such as seagrass beds and coral
yas River estuary in Ecuador, seasonally high river flow and tidal reefs, are especially sensitive to eutrophication (Hatcher et al.,
exchange (3 m) result in a water residence time of only 11 days. 1989; Linden, 1990) considering their need for clear water and
This estuary maintains good water quality, in spite of huge input low ambient concentrations of dissolved and particulate nutrients
of nutrients from both urban and shrimp farming land use (Twilley (D’Elia and Wiebe, 1990; Fourqurean et al., 1993; Alongi, 1998).
et al., 1999, 2001). It has been demonstrated that nutrient enrichment has a nega-
Nitrogen is often considered more limiting to primary produc- tive effect on coral reproduction (Cox and Ward, 2002), and its cal-
tion in coastal marine ecosystems in the temperate zone, while cification, decreasing the growth rate of the reef. This may bring to
phosphorus is thought to be more limiting in tropical coastal sys- algal overgrowth of the reef, with a phase shift coral/macroalgae
tems, although there are many exceptions to these generalities (Pastorok and Bilyard, 1985; McClanahan et al., 2003). Nutrient
(Howarth et al., 1995, 1996). enrichment is also correlated with a major incidence in coral dis-
The role of nutrient limitation may be specific to different types eases (Bruno et al., 2003; Kuntz et al., 2005). Kuntz et al. (2005)
of primary producers, as observed in temperate systems. In tropical show that a chronic stress is more damaging to corals than acute
planktonic marine ecosystems that are offshore, nitrogen is more stress. In our analysis we show that nutrient enrichment in the
limiting to primary production than phosphorus (Howarth, 1988; coastal waters of the island is in act since the beginning of the
Vitousek and Howarth, 1991; Howarth et al., 1995, 1996). Consid- monitoring program, implicating a chronic stress for the adjacent
ering the Caribbean Sea, evidence strongly suggests nitrogen limi- reefs.
tation for planktonic systems (Margalef, 1965; Corredor, 1976, To avoid nutrient enrichment on coral reefs, the biologically
1979; Corredor et al., 1984, 1999). Yet phosphorus rather than available nitrogen (nitrates and ammonia) should be lower than
nitrogen limits primary productivity of macrophyte vegetation 1.0 lM (<0.014 ppm), and the biologically available phosphorous
such as mangroves (Feller, 1995; Twilley, 1995; Koch, 1996) and less than 0.1 lM (<0.003 ppm). Moreover the chlorophyll concen-
seagrasses (Short et al., 1985) under the specific environments that tration should not exceed 0.5 parts per billion (Costa et al., 2008).
they were tested (carbonate geology). In the case of San Andrés, In our case, the nutrient concentration is well above these
most sampling stations shows N:P rates <16:1 in both climatic sea- parameters in all sites. During the dry season, only Punta Hansa,
sons, confirming that in its waters nitrogen is the limiting factor. Rocky Cay and Frente Sharky’s show nitrogen values below
The only site where there is a N:P rate of 70.6, during dry season, 1.0 lM (0.9, 0.9 and 0.7 lM, respectively), while their phosphorous
is Influencia Basurero, where phosphorous is the limiting factor. concentration is equal to 0.1 lM, together with Cabañas Altamar
We may observe that during the rainy season the N:P rate tends and Influencia Basurero. During the wet season, only Frente Shar-
to change in favor of phosphorous, indicating a moderate input ky’s has biological available nitrogen lower than 1.0 lM, while
of this element through land runoff. The concentration of nitrogen, Influencia Basurero has the lowest value of phosphorous
on the other side, tends to diminish, revealing a dilution of its com- (0.1 lM). During the dry season, the mean values for nitrogen
pounds. The origin of nitrogen inputs in the coastal water of the is- range between 3 and 9 folds the maximum values recommended.
land is probably the sewage discharge, which is diluted during the At the site Influencia Basurero, the mean value is 29 lM. Although
rainy season. According to the Bellairs Research Institute (1989, ci- this high mean value is due to the enormous ammonia value de-
ted in Rawlins et al., 1998), non-polluted coastal waters in the tected in 2001, during the other years sampled values were below
Caribbean have nitrite/nitrate concentrations of 0.70, and 0.1 lg/L 10 lg/L, the minimum detectable with the method employed by
of phosphates, compared to values >4 and 0.5–1.5 lg/L, respec- CORALINA. During the wet season, nitrogen values are generally
tively in polluted sites. For San Andrés Island, all sites shows values lower at all sites; nevertheless they are between 2- and 6.4-fold
well above the concentrations reported by that study, indicating a above the limit set for coral reef health. The site Influencia Basure-
nutrient enrichment process. ro has a mean value of 217.4 lM, mainly because during the year
The human impact on coastal water results mostly in a nutrient 2001 it was detected an ammonia concentration of 15,480 lg/L.
enrichment and consequent changes in chlorophyll concentration, However, during the other years sampled, the concentration of
water turbidity, primary productivity, and may induce harmful al- nitrogen was still quite high.
1028 B. Gavio et al. / Marine Pollution Bulletin 60 (2010) 1018–1030

Equally, seagrass beds are adversely affected by nutrient enrich- Some enterovirus are accumulated in coral mucus (Lipp et al.,
ment. In Cartagena Bay, Atlantic Colombia, almost 90% of the beds 2002), even when these pathogens are in concentrations not
were lost in the past 70 years, mainly because of sewage discharge detectable in the water, posing at risk, once again, the health of
and consequent nutrient enrichment (Díaz and Gómez López, people and marine ecosystems.
2003). Generally, the loss of seagrass beds for nutrient enrichment Chaves-Fonnegra et al. (2007), found Escherichia coli in the mu-
is due to an overgrowth of phytoplankton, macroalgae and epi- cus of the coral Montastraea cavernosa in amounts inversely pro-
phytic algae, which diminish the quantity and quality of light portional to the distance from sewage plumes; The
reaching seagrass leaves, lower the seagrass productivity eventu- concentrations of E. coli in the mucus were more than 10-fold high-
ally killing it (Duarte, 1995). Additionally, nutrient enrichment er than in the Florida Keys. The sponge Cliona delitrix, normally
has indirect effects on the bed, such as sediment resuspension associated to organic pollution (Ward-Paige et al., 2005; Chaves-
due to seagrass loss, an increase in the respiration and consequent Fonnegra et al., 2007), is abundant at a distance of the raw sewage
oxidative stress, and anoxia in the sediment (Burkholder et al., discharge (Chaves-Fonnegra et al., 2007).
2007). A significant increase in epiphyte biomass on seagrasses
may be observed even with limited nutrient load (Peterson et al.,
5. Conclusions
2007), emphasizing the sensibility of these ecosystems to anthro-
pogenic impacts.
The coastal waters of San Andrés show signs of nutrification,
with nitrogen and phosporous concentrations well above the limit
4.2. Coliforms (fecal contamination)
set for Caribbean non-polluted waters. The presence of contamina-
tion-loving organisms, such as C. delitrix, in great abundance near
Fecal and total coliforms are considered an indicator of marine
the sewage discharge area, together with high concentrations of
water quality, in terms of fecal and organic matter, as well as min-
pathogenic bacteria, both in the water and in the mucus of stony
eral nutrients (Easterbrook and West, 1987; Charlmers et al., 2000,
corals, should get the attention of the local authorities for a better
both cited in Herrera and Suarez, 2005). The relationship between
management of wastewater. Although there is a common belief
infections and water contaminated by sewage is known since
that the pollutants are rapidly diluted in the open waters around
1854, when Dr. Snow linked the worst cholera epidemics in Lon-
the island, with small or no effect on the coastal ecosystems, evi-
don to the water contaminated by sewage discharge (Dorfman,
dence from this study and others (e.g. Chaves-Fonnegra et al.,
2004).
2007, Mancera et al., in preparation) show that the contaminants,
Several studies have put in evidence the increased risk of gas-
mainly raw sewage, do have a detrimental effect on the coastal
troenteritis, dermatitis, respiratory infections and ear, nose and
water quality and the nearby ecosystems, which are the primary
throat ailments in swimmers bathing in contaminated waters
source of income for the island, both for tourism and fishing.
(p.e. Hunter and Arbona, 1995; Fleisher et al., 1996; Henrickson
It is therefore urgent to take action for a better management of
et al., 2001; Dorfman, 2004). It is estimated that, every year, be-
the sewage wastewater, both with connecting most population to
tween 1.8 and 3.5 millions of infections are caused by swimming
the system, and with a treatment plant prior to ocean disposal.
in sewage polluted waters (http://www.nrdc.org/water/pollution/
sewage.asp), with high medical costs.
The concept that pathogenic bacteria die quickly once in contact Acknowledgements
with seawater does not correspond to reality. The factors deter-
mining the survival and growth of these bacteria in marine waters We wish to thank Tomàs Guerrero, Project Manager ‘‘Protección
are salinity, temperature, predation, sunlight, toxic chemical and y Manejo sostenible del Recurso Hídrico en el Archipiélago”, from
nutrients. Sometimes, the high nutrient content in coastal waters CORALINA for his support and for allowing us to analyze the data
can override the stress of suboptimal salinity and temperature of CORALINA’s monitoring program. We acknowledge Patricia Ab-
(Henrickson et al., 2001). The viruses are even more resistant; they dul, from CORALINA, for providing useful bibliography. We are
can survive longer in seawater and can endure better than bacteria grateful to Shennya Ruíz for her help in editing the figures.
the filtration and purification processes of wastewater treatment This project was co-founded by the research groups Estudios
plants (Henrickson et al., 2001; Lipp and Griffin, 2004). Ambientales del Caribe, and Modelación de Ecosistemas Costeros
As in most Caribbean countries, only a small part of the popula- from Universidad Nacional de Colombia.
tion in San Andrés is connected to the sewage system, and there is
no previous treatment of the wastewater before its disposal to the References
ocean.
Our data show clearly that fecal contamination is worrisome in Alongi, D.M., 1998. Coastal Ecosystem Processes. CRC Press LLC, Boca Raton, FL. p.
several sites of the island, and is above the limits set by law for pri- 419.
APHA – AWWA – WPCF, 1995. Standard Methods for Examination of Water and
mary and secondary contact (Table 2). The situation is critic in Waste Water, 19th ed. Washington, D.C.
Hooker Bay and in Alcantarillado, where the pathogenic bacteria Bianchi, T., Pennock, J., Twilley, R.R., 1999. Biogeochemistry of Gulf of Mexico
are present in high numbers most of the time. Due to its morphol- Estuaries. John Wiley and Sons, New York. p. 428.
Bocquené, G., Franco, A., 2005. Pesticide contamination of the coastline of
ogy, and the quantity of wastewater that directly gets to the bay, Martinique. Marine Pollution Bulletin 51, 612–619.
the pollution in Bahía Hooker is even higher than in front of the Bruno, J.F., Petes, L.E., Harvell, C.D., Hettinger, A., 2003. Nutrient enrichment can
sewage system (Alcantarillado). Other sites, in front of beaches increase the severity of coral diseases. Ecology Letters 6, 1056–1061.
Burke, L., Maidens, J., 2005. Arrecifes en Peligro en el Caribe. World Resources
highly popular among tourists, show high values in some occasions Institute, Washington D.C.. p. 84.
(Tables 2 and 3), evidencing a pollution problem of the coastal Burkholder, J.M., Tomasko, D.A., Touchette, B.W., 2007. Seagrasses and
waters of the island, which may pose at risk the swimmers’ health. eutrophication. Journal of Experimental Marine Biology and Ecology 350, 46–72.
Chaves-Fonnegra, A., Zea, S., Gómez, M.L., 2007. Abundance of the excavating
The Caribbean Sea is emerging as a marine disease ‘‘hot spot”
sponge Cliona delitrix in relation to sewage discharge at San Andrés Island, SW
(Harvell et al., 1999). Sewage contamination is related to higher Caribbean, Colombia. Boletín de Investigaciones Marinas y Costeras 36, 63–78.
coral mortality (Kaczmarsky et al., 2005). The white pox disease Cloern, J.E., 1999. The relative importance of light and nutrient limitation of
of the Caribbean coral Acropora palmata is induced by Serratia mar- phytoplankton growth: a simple index of coastal ecosystem sensitivity to
nutrient enrichment. Aquatic Ecology 33, 3–16.
cescens, a bacterium of the human intestinal flora (Patterson et al., Corredor, J.E., 1976. Aspects of Phytoplankton Dynamics in the Caribbean Sea. FAO
2002). Fisheries Report No. 200, pp. 101–114.
 B. Gavio et al. / Marine Pollution Bulletin 60 (2010) 1018–1030 1029

Corredor, J.E., 1979. Phytoplankton response to low-level nutrient enrichment Howarth, R.W., Jensen, H.S., Marino, R., Postma, H., 1995. Transport to and
through upwelling in the Colombian Caribbean Basin. Deep-Sea Research 26A, processing of P in near-shore and oceanic waters. In: Tiessen, H. (Ed.),
731–741. Phosphorus in the Global Environment. SCOPE 5:4. Wiley and Sons,
Corredor, J.E., Morell, J., Mendez, A., 1984. Dissolved nitrogen, phytoplankton Chichester, pp. 323–345.
biomass and island mass effects in the northeastern Caribbean Sea. Caribbean Howarth, R.W., Billen, G., Swaney, D., Townsend, A., Jaworski, N., Lajtha, K.,
Journal of Science 20, 129–137. Downing, J.A., Elmgren, R., Caraco, N., Jordan, T., Berendse, F., Freney, J.,
Corredor, J.E., Howarth, R.W., Twilley, R.R., Morell, J., 1999. Nitrogen cycling and Kudeyarov, V., Murdoch, P., Zhao-Liang, Z., 1996. Regional nitrogen budgets and
anthropogenic impact in the tropical interamerican seas. Biogeochemistry 46, riverine N and P fluxes for the drainages to the North Atlantic Ocean: natural
163–178. and human influences. Biogeochemistry 35, 75–139.
Costa Jr., O.S., Nimmo, M., Attril, M.J., 2008. Coastal nutrification in Brazil: a review Hunter, J.M., Arbona, S.I., 1995. Paradise lost: an introduction to the geography of
of the role of nutrient excess on coral reef demise. Journal of South American water pollution in Puerto Rico. Social Science and Medicine 40 (10), 1331–1355.
Earth Sciences 257, 270. IDEAM, 1995. Datos de las variables climáticas de la isla de San Andrés, Providencia
Cox, E.F., Ward, Y.S., 2002. Impact of elevated ammonium on reproduction in two y Santa Catalina. Santafé de Bogotá D.C. Colombia, p. 70.
Hawaiian scleractinian corals with different life history patterns. Marine IGAC, 1986. San Andrés y Providencia: Aspectos geográficos. Instituto Geográfico
Pollution Bulletin 44, 1230–1235. Agustín Codazzi. Bogotá D.E., p. 156.
DANE (Departamento Administrativo Nacional de Estadística), 2005. Censo General INVEMAR, 2001. Informe del estado de los ambientes marinos y costeros en
2005. Nivel Nacional. Republica de Colombia, p. 50. Colombia: 2000. Serie Documentos Generales No. 3. Santa Marta, p. 138.
Debrot, A.O., Tiel, A.B., Bradshaw, J.E., 1999. Beach debris in Curaçao. Marine INVEMAR, 2002. Informe del estado de los ambientes marinos y costeros en
Pollution Bulletin 38, 795–801. Colombia: año 2001. In: Ospina-Salazar, G.H., Acero, A. (Eds.), Medellín: Cuartas
D’Elia, C.F., Wiebe, W.J., 1990. Biogeochemical nutrient cycles in coral-reef Impresores (Serie de Publicaciones Periódicas/INVEMAR, no. 8), p. 178.
ecosystems. In: Dubinsky, Z. (Ed.), Ecosystems of the World 25 Coral Reefs. Kaczmarsky, L.T., Draud, M., Williams, E.H., 2005. Is there a relationship between
Elsevier, Amsterdam, pp. 49–74. proximity to sewage effluent and the prevalence of coral disease? Caribbean
Diaz, J.M., Garzón-Ferreira, J., Zea, S., 1995. Los Arrecifes coralinos de la isla de San Journal of Science 41 (1), 124–137.
Andrés, Colombia: Estado actual y perspectivas para su conservación. Academia Kingsbury, P., 2005. Jamaican tourism and the politics of enjoyment. Geoforum 36,
Colombiana de Ciencias exactas, físicas y naturales, Colección Jorge Alvarez 113–132.
Lleras No. 7. Kjerfve, B., Drude De Lacerda, L., Dias, G.T.M., 2001a. Baia de Guanabara, Rio de
Díaz, J.M., Gómez López, D.I., 2003. Cambios históricos en la distribución y Janeiro, Brazil. In: Seeliger, U., Kjerve, B.J. (Eds.), Coastal Marine Ecosystems of
abundancia de praderas de pastos marinos en la bahía de Cartagena y áreas Latin America. Springer-Verlag, New York. pp. 107–118.
aledañas (Colombia). Boletín de Investigaciones Marinas y Costeras 32, 57–74. Kjerfve, B., Seeliger, U., Drude De Lacerda, L., 2001b. A summary of natural and
Diaz, J.M., Díaz-Pulido, G., Garzón-Ferreira, J., Geister, J., Sanchez, J., Zea, S., 1996. human-induced variables in coastal marine ecosystems of Latin America. In:
Atlas de los arrecifes coralinos del Caribe colombiano. I complejos arrecifales Seeliger, U., Kjerve, B.J. (Eds.), Coastal marine ecosystems of Latin America.
oceánicos. INVEMAR, Santa Marta. p. 29. Springer-Verlag, New York. pp. 341–354.
Dorfman, M., 2004. Swimming in sewage, the growing problem of sewage pollution Koch, M.S., 1996. Resource availability and abiotic stress effects on Rhizophora
and how the Bush administration is putting our health and environment at risk. mangle L. (red mangrove) development in south Florida. Ph.D. Dissertation.
Natural Resources Defense Council and the Environmental Integrity Project 1, 75. University of Miami, Coral Gables, Florida, p. 134.
Duarte, C.J., 1995. Submerged aquatic vegetation in relation to different nutrient Kuntz, N.M., Kline, D.I., Sandin, S.A., Rohwer, F., 2005. Pathologies and mortality
regimes. Ophelia 41, 87–112. rates caused by organic carbon and nutrient stressors in three Caribbean coral
Dudgeon, D., 1992. Endangered ecosystems: a review of the conservation status of species. Marine Ecology Progress Series 294, 173–180.
tropical Asian rivers. Hydrolobiologia 248, 167–191. Linden, O., 1990. Human impact on tropical coastal zones. Nature Resources 26 (4),
Feller, I.C., 1995. Effects of nutrient enrichment on growth and herbivory of dwarf 3–11.
red mangrove (Rhizophora mangle). Ecological Monographs 65, 477–505. Lipp, E.K., Griffin, D.W., 2004. Analysis of coral mucus as an improved medium for
Fleisher, J.M., Kav, D., Salmon, R.L., Jonies, F., Wyer, M.D., Godfree, A.F., 1996. Marine detection of enteric microbes and for determining patterns of sewage
waters contaminated with domestic sewage: nonenteric illnesses associated contamination in reef environments. EcoHealth 1, 317–323.
with bather exposure in the United Kingdom. American Journal of Public Health Lipp, E.K., Jarrell, J.L., Griffin, D.W., Lukasik, J., Jacukiewicz, J., Rose, J.B., 2002.
86 (9), 1228–1234. Preliminary evidence for human fecal contamination in corals of the Florida
Fourqurean, J.W., Jones, R.D., Zieman, J.C., 1993. Processes influencing water column Keys, USA. Marine Pollution Bulletin 44 (7), 666–670.
nutrient characteristics and phosphorus limitation of phytoplankton biomass in Lonin, S., Mendoza, L., 1997. Evaluacion hidrodinámica de las bahías Hooker e
Florida Bay, FL, USA: inferences from spatial distributions. Estuarine, Coastal Icacos. Boletín científico CIOH 18, 51–64.
and Shelf Science 36, 295–314. Mancera, J.E., Guerra, L., Ruiz, S.C., Malo, M.A., Pérez, S.P. Evaluación del impacto de
Garay, J., Castro, L., 1993. Niveles de hidrocarburos del petróleo en la isla de San los vertimientos del emisario submarino de San Andrés isla sobre las
Andrés Caribe colombiano 1992. Boletín Científico CIOH 13, 85–101. comunidades planctónicas a partir de variables fisicoquímicas., in preparation.
Garay, J., Castillo, F., Andrade, C., Aguilera, J., Niño, L., De La Pava, M., López, W., Margalef, R., 1965. Composicion y distribucion del fitoplancton. In: Estudios sobre el
Márquez, G., 1988. Estudio oceanográfico del área insular y oceánica del Caribe Ecosistema Pelagico del N.E. de Venezuela. Memoria de la Fundación La Salle de
colombiano – archipiélago de San Andrés y Providencia y cayos vecinos. Boletín Ciencias Naturales 25, 141–208.
Científico CIOH 9, 3–73. Marín, B., 2001. Proyecto Establecimento de valores indicativos del grado de
Garay, J., Panizzo, L., Ramirez, G., Lesmes, L., 2001. Anexo 3. Manual de técnicas contaminación de tóxicos químicos y microorganismos de origen fecal, como
analiticas de parametros fisicoquimicos, contaminantes marinos y base para la expedición de normativas de la calidad de las aguas marinas de
microbiologicos en aguas marinas y costeras. In: INVEMAR (Ed.), Diagnostico Colombia. COLCIENCIAS. Informe final. Santa Marta.
y evaluación de la calidad ambiental marina en el Caribe y Pacifico colombiano. Marín, B., Cadavid, B., 2001. Descripción general de la calidad de las aguas marinas
Red de vigilancia para la conservación y protección de las aguas marinas y de Colombia. Caracterización de la calidad de las aguas marinas. Informe
costeras de Colombia. Informe técnico final. Tomo I. Santa Marta, pp. 1–74. técnico. Santa Marta, p. 80.
Geister, von J., 1975. Riffbau und geologische Entwicklungsgeschichte der Insel San McClanahan, T.R., Sala, E., Stickels, P.A., Cokos, B.A., Baker, A.C., Starger, C.J., Jones IV,
Andrés (westliches Karibisches Meer, Kolumbien). Stuttgarter Beiträge zur S.H., 2003. Interaction between nutrients and herbivory in controlling algal
Naturkunde, Serie B. Nr. 15. communities and coral condition on Glover’s Reef, Belize. Marine Ecology
Harborne, A.R., Afzal, D.C., Andrews, M.J., 2001. Honduras: Caribbean coast. Marine Progress Series 261, 135–147.
Pollution Bulletin 42 (12), 1221–1235. Mignucci-Giannoni, A.A., 1999. Assessment and rehabilitation of wildlife affected by
Harvell, C.D., Kim, K., Burkholder, J.M., Colwell, R.R., Epstein, P.R., Grimes, D.J., an oil spill n Puerto Rico. Environmental Pollution 104, 323–333.
Hofmann, E.E., Lipp, E.K., Osterhaus, A.D.M.E., Overstreet, R.M., Porter, J.W., Ministerio de Protección Social, Republica de Colombia, 1984. Decreto 1594 de
Smith, G.W., Vasta, G.R., 1999. Emerging marine diseases-climate links and 1984. <http://www.minproteccionsocial.gov.co/VBeContent/library/documents/
anthropogenic factors. Science 285, 1505–1510. DocNewsNo16115DocumentNo4054.PDF> (accessed 22.02.09).
Hatcher, B.G., Johannes, R.E., Robertson, A.I., 1989. Review of research relevant to Odum, H.T., Copeland, B.J., McMahan, E., 1972. Coastal Ecosystems of the United
the conservation of shallow tropical marine ecosystems. Oceanography Marine States, vols. 1–4. Conservation Foundation.
Biology Annual Review 27, 337–414. Panke, M., Quimby, S., 2000. Pesticides. Caribbean Currents 8 (3), 1–5.
Heisler, J., Glibert, P.M., Burkholder, J.M., Anderson, D.M., Cochlan, W., Dennison, Pastorok, R.A., Bilyard, G.R., 1985. Effects of sewage pollution on coral-reef
W.C., Dortch, Q., Gobler, C.J., Heil, C.A., Humphries, E., Lewitus, A., Magnien, R., communities. Marine Ecology Progress Series 21, 175–189.
Marshallm, H.G., Sellner, K., Stockwell, D.A., Stoecker, D.K., Suddleson, M., 2008. Patterson, K.L., Porter, J.W., Ritchie, K.B., Polson, S.W., Mueller, E., Peters, E.C.,
Eutrophication and harmful algal blooms: a scientific consensus. Harmful Algae Santavy, D.L., Smith, G.W., 2002. The etiology of white pox, a lethal disease of
8, 3–13. the Caribbean elkhorn coral, Acropora palmata. PNAS 99 (13), 8725–8730.
Henrickson, S.E., Wong, T., Allen, P., Ford, T., Epsteins, P.R., 2001. Marine swimming- Pennock, J.R., Boyer, J.N., Herrera-Silveira, J.A., Iverson, R.L., Whitledge, T.E.,
related illness: implications for monitoring and environmental policy. Mortazavi, B., Comin, F.A., 1999. Nutrient behavior and phytoplankton
Environmental Health Perspectives 109 (7), 645–650. production in Gulf of Mexico Estuaries. In: Bianchi, T., Pennock, J., Twilley, R.
Herrera, A., Suarez, P., 2005. Indicadores bacterianos como herramienta para medir (Eds.), Biogeochemistry of Gulf of Mexico Estuaries. John Wiley and Sons. pp.
la calidad ambiental del agua costera. Asociación Interciencia 30 (003), 171– 109–162.
176. Peterson, B.J., Frankovich, T.A., Zieman, J.C., 2007. Response of seagrass epiphyte
Howarth, R.W., 1988. Nutrient limitation of net primary production in marine loading to field manipulations of fertilization, gastropod grazing and leaf
ecosystems. Annual Review of Ecology 19, 89–110. turnover rates. Journal of Experimental Marine Biology and Ecology 349, 61–72.
1030 B. Gavio et al. / Marine Pollution Bulletin 60 (2010) 1018–1030

Rawlins, B.G., Ferguson, A.J., Chilton, P.J., Arthurton, R.S., Rees, J.G., Baldock, J.W., Twilley, R.R., 1995. Properties of mangrove ecosystems related to the energy signature
1998. Review of agricultural pollution in the Caribbean with particular of coastal environments. In: Hall, C.A.S. (Ed.), Maximum Power: The Ideas and
emphasis on small island developing states. Marine Pollution Bulletin 36 (9), Applications of H.T. Odum. University Press of Colorado, Niwot, CO, pp. 43–62.
658–668. Twilley, R.R., Cowan, J., Miller-Way, T., Montagna, P., Mortazavi, B., 1999. Benthic
Short, F.T., Davis, M.W., Gibson, R.A., Zimmermann, C.F., 1985. Evidence for fluxes of selected estuaries in the Gulf of Mexico. In: Bianchi, T., Pennock, J.,
phosphorus limitation in carbonate sediments of the seagrass syringodium Twilley, R. (Eds.), Biogeochemistry of Gulf of Mexico Estuaries. John Wiley and
filiforme. Estuarine, Coastal and Shelf Science 20, 419–430. Sons. pp. 163–209.
SIGAM/CORALINA, 2004. Agenda ambiental de San Andrés Islas (on line). <http:// Twilley, R.R., Cárdenas, W., Rivera-Monroy, V.H., Espinoza, J., Suescum, R., Armijos,
www.coralina.gov.co/archivos/Sigam_CAPITULO%20_I_Perfil_Ambiental_1.pdf> M.M., Solórzano, L., 2001. Ecology of the Gulf of Guayaquil and the Guayas River
(Fecha de consulta 29/10/2007). Estuary. In: Seeliger, U., Kjerve, B.J. (Eds.), Coastal Marine Ecosystems of Latin
Siung-Chang, A., 1997. A review of marine pollution issues in the Caribbean. America. Springer-Verlag, New York, p. 360 (pp. 245–263).
Environmental Geochemistry and Health 19, 45–55. Vitousek, P.M., Howarth, R.W., 1991. Nitrogen limitation on land and in the sea:
Steer, R., Arias, F.A., Ramos, A., Sierra, P.C., Alonso, D.A., Ocampo, P., 1997. how can it occur? Biogeochemistry 13, 87–115.
Documento base para la elaboración de la política nacional de ordenamiento Ward-Paige, C.A., Risk, M.J., Sherwood, O.A., Jaap, W.C., 2005. Clionid sponge surveys
integrado de las zonas costeras. Documento de consultoría. INVEMAR. Serie on the Florida Reef Tract suggest land-based nutrient inputs. Marine Pollution
Publicaciones Especiales 6, 395. Bulletin 51, 570–579.