Marine Pollution Bulletin 60 (2010) 1018–1030

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Marine Pollution Bulletin

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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
The Caribbean is the world’s region most dependent of tourism
(Kingsbury, 2005), with the typical attraction of ‘‘sun, sand and
sea”, where visitors are attracted by the pristine conditions of its
coasts. Therefore, marine pollution problems are particularly men-
acing in this area. The Caribbean coastal area has not reached, yet,
pollution levels seen in other regions (Harborne et al., 2001). How-
ever, in the last 20–30 years, marine pollution and coastal degrada-
tion have become serious issues (Siung-Chang, 1997).
As previous studies have revealed, the main polluting problems
of the coastal waters in the Caribbean are oil spills and untreated
sewage pollution, followed by solid wastes (mainly domestic),
industrial pollution and pesticides (Siung-Chang, 1997; Debrot
et al., 1999; Mignucci-Giannoni, 1999; Harborne et al., 2001; Boc-
quené and Franco, 2005). These problems are emphasized by the
fact that the Caribbean Sea is a closed basin with little water ex-
change (Atwood, 1977, cited in Panke and Quimby, 2000), making
it an ideal place for the accumulation of pollutants (Panke and Qui-
mby, 2000).
San Andrés Island is part of the San Andrés, Old Providence and
Santa Catalina Archipelago, and lays in the Caribbean region,
* Corresponding author. Address: Departamento de Biología, Universidad Nac-
ional de Colombia, Sede Bogotá, Ciudad Universitaria, Edificio, 421 Bogotá, D.C.,
Colombia. Tel.: +57 8 5133310; fax: +57 8 5133310x15.
E-mail address: bgavio@yahoo.com (B. Gavio).
290 km off the coast of Nicaragua and 480 km off the coast of
Cartagena (Colombia).
The island has an area of 25 km2; with a resident population of
55.426 habitants (DANE, 2005), equivalent to 2217.04 habitants/
km2, it is maybe the most densely populated island of the Carib-
bean (Diaz et al., 1996). In 2001 the whole archipelago was de-
clared by UNESCO a Biosphere Reserve, under the supervision of
the Corporation for the Sustainable Development of San Andrés,
Old Providence and Santa Catalina Archipelago, CORALINA.
The island’s major incomes are tourism and commerce, fol-
lowed by fishery. San Andrés fits well as a typical Caribbean insular
country: it is highly dependent on tourism, its population in-
creased with little or no land planification, leading to a chaotic
coastal development, the sewage system covers only 8% of the res-
ident population (SIGAM/CORALINA, 2004), without any treatment
prior to its disposal into the ocean.
The great majority of the population wastewater is disposed in
septic tanks, but its leaking has polluted not only great part of the
drinking water wells of the island, is also impacting heavily its
nearshore waters and ecosystems (Marín and Cadavid, 2001).
It has been estimated that a total of 14.466 m3 of untreated
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 
1018 NMP/day of fecal coliforms (INVEMAR, 2002).
Other polluting fonts are the inadequate solid waste disposal, in
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
coast, illegal oil spill from boats, and deterioration of mangrove
ecosystems (Marín, 2001; INVEMAR, 2001). The overexploitation
of the marine resource is another important concern in the island,
and is severely putting at risk the coral reefs nearby (Burke and
Maidens, 2005).
CORALINA, the highest environmental authority of the Archipel-
ago, started a water quality monitoring program of the coastal
water of the island in 1997. There are no formal studies prior to
the monitoring program on the coastal water quality of the island,
being the monitoring program run by CORALINA part of REDCAM,
(Red de vigilancia para la conservación y protección de las aguas
marinas y costeras de Colombia), directed by INVEMAR (Instituto
de Investigaciones Marinas y Costeras ‘‘José Benito Vives de And-
réis”). This lack of previous data, extended to the entire country,
is due partially to a historical lack of interest of Colombia to its
sea and its resources (Steer et al., 1997; INVEMAR, 2001). Only in
1993, the environmental authorities in the country (the Ministry
of Environment and the Regional Autonomous Corporations for
Sustainable Development) were created, and few years later
(2000) the Environmental Politic for Coastal Zones was finally
established (INVEMAR, 2001).
The objective of the present paper is to provide the first analysis
of the monitoring data of CORALINA, in the time span 2000–2005.
We hope the present work will help to better understand the cur-
rent situation of the coastal waters of San Andrès Island, and pro-
Fig. 1. The island of San Andrés in the Caribbean Sea showing sample site location.
1019
vide better tools for the environmental management of its marine
resources.
2. Materials and methods
2.1. Study site
San Andrès is a small island (25 km2) (Fig. 1) that lies between
12°280 5800 and 12°350 5500 N and 81°40’4900 and 81°430 2300 W (IGAC,
1986). It forms part of the Archipelago of San Andrès, Providencia
and Santa Catalina, and it is the administrative center of the
Department, and the main touristic target. The population is con-
centrated in the northern part of the island (around 7000 habi-
tants/km2), as well as the tourism. Towards the center and the
south, the population density is much lower and the island still
maintains rural characteristics.
The island, and the rest of the archipelago, is volcanic in origin.
The subsidence of the volcanic base, and its simultaneous cover
with calcareous deposits, biogenic in origin, during the Tertiary
and Quaternary, gave rise to the present island (Diaz et al., 1996).
The marine platform on the oriental side is shallow, and gets to
the coral reefs in the open ocean, which mitigate the waves. On this
submarine terrace there are deposits of corals, coralline algae,
urchins and other animals, which produce calcareous sand
(Geister, 1975).
1020 B. Gavio et al. / Marine Pollution Bulletin 60 (2010) 1018–1030
On the west side of the island, the transition is much more
abrupt, with cliffs indicating strong marine erosion (IGAC, 1986).
The island lies in the transition zone between tropical dry and
tropical wet climate. The influence of trade winds mitigates the
dry and warm climate. The annual mean temperature is 27.4 °C,
with maximum values between 29 and 30 °C (May–June) and min-
imum between 25.5 and 26.0 °C (December–February). The annual
mean precipitation is 1797.8 mm, unevenly distributed in a dry
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,
1995).
The predominant currents around San Andres Island are caused
by the north-east trade winds (Díaz et al., 1995). Currents intercept
the island from the northeast, running through the barrier reef and
diverging to the south of the island. Current velocity is reduced by
the barrier reef and becomes weaker on the western coast of the
island (Díaz et al., 1995). Waves formed in the open sea break di-
rectly on to the barrier reef, and diffract around the island.
Fig. 2. Nitrate concentration (lg/L). A–C dry season. D–F wet season.
Along the northeast coast of the island the currents are slow,
with the maximum speed (10 m/min) close to the reef. In the pro-
tected areas the current velocity does not exceed 4–5 m/min, with
the same wind conditions (Garay and Castro, 1993).
The archipelago is influenced by the Caribbean current which
originates temporal convergent whirlpools affecting the distribu-
tion and concentration of plankton and associated nutrients (Garay
et al., 1988).
2.2. Monitoring protocol
CORALINA, the corporation responsible of monitoring the coast-
al water quality of the Archipelago, started the monitoring pro-
gram in 1997, as part of the program REDCAM of the INVEMAR.
They sample twice a year, once during the dry season (January–
May), and once during the wet season (June–December), in 14 sites
around the island (Fig. 1), 60 m off the coast, at a water depth of
30 cm.
 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
in northern portion of the island, in front of the most populated
beaches and the center of the town. Cabañas Altamar is in front
of a district less populated than the center, on the western side
of the island. Alcantarillado is where the sewage system gets to
the sea, however, since September 2007 there is a submarine sys-
tem which brings the wastewater offshore, on the western side of
the island. El Cove is a small closed bay, once a harbor for the army;
Yellow Moon and Rocky Cay are sites in front of two hotels on the
eastern coast, but the area here is much less populated than the
north. Bahía Hooker is an enclosed bay, which in the past has been
under heavy anthropogenic pressure (Lonin and Mendoza, 1997).
In 1961, an electric plant was installed here, and the water used
to refrigerate the plant was directly discharged in the bay, together
with oil and combustible of the same plant. In 1974, a district of
approximately 75 houses was built close by, and all the sewage
discharges were, and still are, directly released in the bay. In
1996, the harbor was built north to the bay, and the communica-
tion of the bay with the open water was reduced to a shallow
and narrow channel, reducing even more its hydrodynamics and
consequent water exchange. The bay is surrounded by a mangrove
wetland, which has been declared regional park (Mangrove Regio-
nal Park Old Point) by CORALINA in 2002, together with the bays.
In Bahía Hooker CORALINA has two sampling sites, one inside
the bay, where mangroves are, and one where the electric plant
once was. Muelle is the harbor of the island, where large boats ar-
rive daily to bring the comestible goods and other merchandise to
the island (almost all the goods are imported from mainland).
Johnny Cay is a small rocky islet, in front of the northern part of
the island, where tourists go to spend the day. The islet is not per-
manently inhabitated, but few restaurants are active daily to re-
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-
posal system of the island gets to the ocean. Finally, Frente Sharky’s
is also on the west coast of the island, where few houses are
inhabitated.
In each site, they collect water samples to determine nitrites, ni-
trates, ammonia, phosphates, fecal coliforms and total coliforms.
The water samples were collected in plastic bottles (500 ml)
and transported (refrigerated to 4 °C) to the laboratory. For nutri-
ent analysis, they follow APHA protocols (APHA, 1995; Garay
et al., 2001). The analyses were run on a spectrophotometer Spec-
tronic 5 Genesys, with a minimum detection range of 2 lg/L.
To determine the number of coliforms, they used the method of
colony formation (membrane filtering) until 2000. In 2001, they
changed to the more probable number (both techniques described
in Garay et al., 2001). They also measure other parameters, (tem-
perature, salinity, pH, etc.). However, the present paper focuses
exclusively on the nutrient and coliform analysis, which was
started in 2000.
3. Results
3.1. Nitrites
Nitrites concentration was below the minimum detectable
(2 lg/L) most of the time at all sites (data not shown). Only in
Alcantarillado, Hooker Bay (both sites) and Influencia Basurero
the registered values are above the minimum detectable for some
years. In Alcantarillado, concentrations of 3 lg/L were detected for
the dry season of 2001 and 2002, 5 lg/L in the dry season of 2004
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
Basurero showed an anomalous concentration of 524 lg/L
(Fig. 2a) while the other years sampled, in the dry season, values
were always below 100 lg/L. In 2000, during the wet season, the
highest values of nitrate were recorded for most sites (Fig. 2d
and f) with the exception of Yellow Moon (Fig. 2e), Jhonny Cay
and the Cove (Fig. 2f).
3.3. Ammonia
Ammonia concentration are generally lower in dry season
(Fig. 3a–c) than during wet season (Fig. 3d–f). During dry season,
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
in 2001 anomalous values of 137 and 1900 lg/L were registered for
Alcantarillado and Influencia Basurero, respectively. In 2002,
Alcantarillado had a value of 405.6 lg/L (Fig. 3a). During 2003
Fig. 4. Phosphate concentration (lg/L). A–C dry season. D–F wet season.
and 2004, at all sites the ammonia concentration were below
10 lg/L; only Alcantarillado recorded 14 lg/L in 2004.
During wet season, ammonia values are generally higher, and
range between 13 and 95 lg/L (Fig. 3d–f). In Punta Hansa, Isleño,
Punta Norte and Rocky Cay, no data were taken in 2000 (Fig. 3f).
As in the dry season, in 2001 abnormal values were detected in
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
were below 10 lg/L, while the following year ammonia concentra-
tions were high everywhere, ranging between 47 and 69 lg/L. In
general terms, ammonia concentration is considerably higher dur-
ing wet season, than during dry season (Fig 3).
3.4. Phosphates
During dry season, phosphate concentration generally range be-
tween 8 and 60 lg/L (Fig. 4a–c), with anomalous values of 179 and
 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
season, phosphate values are generally higher, ranging from 8 to
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
of 2003 showed higher values of phosphates at all sites.
3.5. N:P ratio
During the dry season, the relationship N:P is generally low,
ranging from 2.3 (Rocky Cay) to 16.9 (Cabañas Altamar), evidenc-
ing that the primary productivity is limited by nitrogen in these
waters. Only Influencia Basurero has a relationship N:P of 58.5,
indicating that P is the limiting factor. During the rainy season,
the N:P is even lower, ranging from 1.4 (Hooker Bay, plant) to
6.4 (Influencia Basurero) (Table 1).
3.6. Fecal coliforms
Only since 2001, the counting of coliforms (fecal and total) are
expressed as more probable number (MPN)/100 mL. From 1997
to 2000, they were estimated as colony-forming units (CFU). There-
fore, we only present the data from 2001 to 2005, since the two
methods are not comparable. Hotel Isleño presents counting of
210 NMP/100 mL during both seasons of 2001 (Table 2). In Punta
Norte 11,000 NMP/100 ML were detected in the rainy season of
2001. Alcantarillado has high values during most of the sampling,
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/
100 mL were detected in the rainy season of 2001, Hooker Bay
(mangrove) revealed high numbers in 2001 (both seasons) 2003
dry season and 2004 rainy season. The other site in Hooker Bay
(plant) had high concentrations of fecal coliforms (ranging
from 210 to >16,000 NMP/100 mL) during the whole time log
examined, with the only exception of the rainy season of 2002,
when 60 NMP/100 mL were detected.
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
coliform counting is higher during the dry season. In Colombia, the
decreto 1594 of 1984 determines the maximum limits of fecal and
total contaminants in coastal waters for recreational use. For fecal
contamination, the maximum limit for primary contact is 200
NMP/100 mL, while there is no limit assigned for secondary
contact.
3.7. Total coliforms
According to the law (Decreto 1594 of 1984, Ministerio de Pro-
tección Social, 1984), the maximum limits for total coliform in rec-
reational waters are the following: 1000 NMP/100 mL for primary
contact and 5000 NMP/100 ML for secondary contact. These limits
are passed by several sites particularly in 2001 (both seasons),
2003 (dry season) and 2004 (rainy season) (Table 3). The sites most
contaminated are Alcantarillado, where limits were passed every
year with the exception the rainy season of 2003 and 2005; Hooker
Bay (mangrove) where counting were always above the limits,
with the exception of 2003 (rainy season) 2004 (dry season) and
2005 (dry season); and Hooker Bay (plant) where the limits were
not passed only in 2002 (rainy season) 2003 (rainy season) 2004
(dry season) and 2005 (rainy season). As for the fecal coliforms,
during the dry season there is a major concentration of total coli-
forms than during the rainy season.
4. Discussion
4.1. Nutrients
Several recent reviews found that tropical marine ecosystems
do not fit the established eutrophication paradigm currently ap-
plied to management decisions (Bianchi et al., 1999; Pennock
et al., 1999). Few models, mass budgets, and synoptic measures
of processes are known for tropical polluted marine ecosystems
(Dudgeon, 1992). The amounts of solar, mechanical (wind, tides
and waves), and chemical energies together with regional geomor-
phology, establish the template from which site-specific patterns
of primary productivity develop for marine ecosystems (Odum
et al., 1972). Light availability, residence time and nutrient inputs,
which are controlled by the geomorphology and geophysical pro-
cesses, are three key factors limiting primary productivity among
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
with low nutrients and long water residence time, have very clear
waters and low wave energies that support productive seagrass
and coral communities, but low phytoplankton production. In
addition, these environments usually have a limited intertidal wet-
land: water surface area ratio. The response of each type of primary
producer to nutrient enrichment will determine the susceptibility
to eutrophication in each coastal setting.
Suspended load and light are two important factors related to
the response of marine systems to nutrient over-enrichment
(Cloern, 1999). Light levels can play a critical role in response of
systems to nutrient loading, and there is certainly high incident
light year round in tropical latitudes. During peak discharge, total
suspended solid concentrations are high in the coastal zone, but
are lower in dry season. These differences in water clarity between
wet and dry season are important in regulating patterns of primary
productivity.
Residence time of water in coastal zone is an important factor
relating loading rates to ecological processes. High tidal energy
prevents the development of eutrophication in spite of sewage
waste from urban watersheds. Thus, the relatively rapid water re-
newal (11.4 days for the renewal of 50% of the bay water volume)
explains why Baia de Guanabara in Brazil has reasonable water
quality in the lower parts of the bay where huge quantities of un-
treated sewage are discharged (Kjerfve et al., 2001a, b). In the Gua-
yas River estuary in Ecuador, seasonally high river flow and tidal
exchange (3 m) result in a water residence time of only 11 days.
This estuary maintains good water quality, in spite of huge input
of nutrients from both urban and shrimp farming land use (Twilley
et al., 1999, 2001).
Nitrogen is often considered more limiting to primary produc-
tion in coastal marine ecosystems in the temperate zone, while
phosphorus is thought to be more limiting in tropical coastal sys-
tems, although there are many exceptions to these generalities
(Howarth et al., 1995, 1996).
The role of nutrient limitation may be specific to different types
of primary producers, as observed in temperate systems. In tropical
planktonic marine ecosystems that are offshore, nitrogen is more
limiting to primary production than phosphorus (Howarth, 1988;
Vitousek and Howarth, 1991; Howarth et al., 1995, 1996). Consid-
ering the Caribbean Sea, evidence strongly suggests nitrogen limi-
tation for planktonic systems (Margalef, 1965; Corredor, 1976,
1979; Corredor et al., 1984, 1999). Yet phosphorus rather than
nitrogen limits primary productivity of macrophyte vegetation
such as mangroves (Feller, 1995; Twilley, 1995; Koch, 1996) and
seagrasses (Short et al., 1985) under the specific environments that
they were tested (carbonate geology). In the case of San Andrés,
most sampling stations shows N:P rates <16:1 in both climatic sea-
sons, confirming that in its waters nitrogen is the limiting factor.
The only site where there is a N:P rate of 70.6, during dry season,
is Influencia Basurero, where phosphorous is the limiting factor.
We may observe that during the rainy season the N:P rate tends
to change in favor of phosphorous, indicating a moderate input
of this element through land runoff. The concentration of nitrogen,
on the other side, tends to diminish, revealing a dilution of its com-
pounds. The origin of nitrogen inputs in the coastal water of the is-
land is probably the sewage discharge, which is diluted during the
rainy season. According to the Bellairs Research Institute (1989, ci-
ted in Rawlins et al., 1998), non-polluted coastal waters in the
Caribbean have nitrite/nitrate concentrations of 0.70, and 0.1 lg/L
of phosphates, compared to values >4 and 0.5–1.5 lg/L, respec-
tively in polluted sites. For San Andrés Island, all sites shows values
well above the concentrations reported by that study, indicating a
nutrient enrichment process.
The human impact on coastal water results mostly in a nutrient
enrichment and consequent changes in chlorophyll concentration,
water turbidity, primary productivity, and may induce harmful al-
1027
gal blooms (Heisler et al., 2008), with all its consequences. Dis-
solved nutrient concentrations are usually much lower in tropical
surface waters than in temperate waters. An increase of phospho-
rus concentrations by 0.75 lM in an estuary along the Atlantic
coast of North America may increase the concentration 2-fold.
Yet that same concentration increase in a tropical estuary, say in
the Caribbean Sea, would be approximately a 40-fold increase.
The implications of this for tropical community structure and func-
tion are not clear, but the possibility exists that the impact of a gi-
ven increase in nutrient concentrations on a nutrient-poor tropical
marine community might be much greater than that on a typical
temperate marine community (Hatcher et al., 1989).
Nutrient enrichment will enhance net primary productivity par-
ticularly in those environmental settings with high light and longer
residence time of water, such as marine-dominated embayments.
Nutrient loadings that include a decrease in N:P ratios will
disproportionately increase productivity in carbonate systems as
phosphorus becomes more available. Reef and lagoons are
marine-dominated embayments with clear waters that have a long
residence time; yet these waters are oligotrophic usually with
higher N:P ratios. These are sites of high seagrass distribution
and productivity, with limited phytoplankton production and
reduced inputs from mangrove wetlands. Tropical habitats in
marine-dominated embayments, such as seagrass beds and coral
reefs, are especially sensitive to eutrophication (Hatcher et al.,
1989; Linden, 1990) considering their need for clear water and
low ambient concentrations of dissolved and particulate nutrients
(D’Elia and Wiebe, 1990; Fourqurean et al., 1993; Alongi, 1998).
It has been demonstrated that nutrient enrichment has a nega-
tive effect on coral reproduction (Cox and Ward, 2002), and its cal-
cification, decreasing the growth rate of the reef. This may bring to
algal overgrowth of the reef, with a phase shift coral/macroalgae
(Pastorok and Bilyard, 1985; McClanahan et al., 2003). Nutrient
enrichment is also correlated with a major incidence in coral dis-
eases (Bruno et al., 2003; Kuntz et al., 2005). Kuntz et al. (2005)
show that a chronic stress is more damaging to corals than acute
stress. In our analysis we show that nutrient enrichment in the
coastal waters of the island is in act since the beginning of the
monitoring program, implicating a chronic stress for the adjacent
reefs.
To avoid nutrient enrichment on coral reefs, the biologically
available nitrogen (nitrates and ammonia) should be lower than
1.0 lM (<0.014 ppm), and the biologically available phosphorous
less than 0.1 lM (<0.003 ppm). Moreover the chlorophyll concen-
tration should not exceed 0.5 parts per billion (Costa et al., 2008).
In our case, the nutrient concentration is well above these
parameters in all sites. During the dry season, only Punta Hansa,
Rocky Cay and Frente Sharky’s show nitrogen values below
1.0 lM (0.9, 0.9 and 0.7 lM, respectively), while their phosphorous
concentration is equal to 0.1 lM, together with Cabañas Altamar
and Influencia Basurero. During the wet season, only Frente Shar-
ky’s has biological available nitrogen lower than 1.0 lM, while
Influencia Basurero has the lowest value of phosphorous
(0.1 lM). During the dry season, the mean values for nitrogen
range between 3 and 9 folds the maximum values recommended.
At the site Influencia Basurero, the mean value is 29 lM. Although
this high mean value is due to the enormous ammonia value de-
tected in 2001, during the other years sampled values were below
10 lg/L, the minimum detectable with the method employed by
CORALINA. During the wet season, nitrogen values are generally
lower at all sites; nevertheless they are between 2- and 6.4-fold
above the limit set for coral reef health. The site Influencia Basure-
ro has a mean value of 217.4 lM, mainly because during the year
2001 it was detected an ammonia concentration of 15,480 lg/L.
However, during the other years sampled, the concentration of
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-
ment. In Cartagena Bay, Atlantic Colombia, almost 90% of the beds
were lost in the past 70 years, mainly because of sewage discharge
and consequent nutrient enrichment (Díaz and Gómez López,
2003). Generally, the loss of seagrass beds for nutrient enrichment
is due to an overgrowth of phytoplankton, macroalgae and epi-
phytic algae, which diminish the quantity and quality of light
reaching seagrass leaves, lower the seagrass productivity eventu-
ally killing it (Duarte, 1995). Additionally, nutrient enrichment
has indirect effects on the bed, such as sediment resuspension
due to seagrass loss, an increase in the respiration and consequent
oxidative stress, and anoxia in the sediment (Burkholder et al.,
2007). A significant increase in epiphyte biomass on seagrasses
may be observed even with limited nutrient load (Peterson et al.,
2007), emphasizing the sensibility of these ecosystems to anthro-
pogenic impacts.
4.2. Coliforms (fecal contamination)
Fecal and total coliforms are considered an indicator of marine
water quality, in terms of fecal and organic matter, as well as min-
eral nutrients (Easterbrook and West, 1987; Charlmers et al., 2000,
both cited in Herrera and Suarez, 2005). The relationship between
infections and water contaminated by sewage is known since
1854, when Dr. Snow linked the worst cholera epidemics in Lon-
don to the water contaminated by sewage discharge (Dorfman,
2004).
Several studies have put in evidence the increased risk of gas-
troenteritis, dermatitis, respiratory infections and ear, nose and
throat ailments in swimmers bathing in contaminated waters
(p.e. Hunter and Arbona, 1995; Fleisher et al., 1996; Henrickson
et al., 2001; Dorfman, 2004). It is estimated that, every year, be-
tween 1.8 and 3.5 millions of infections are caused by swimming
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
with seawater does not correspond to reality. The factors deter-
mining the survival and growth of these bacteria in marine waters
are salinity, temperature, predation, sunlight, toxic chemical and
nutrients. Sometimes, the high nutrient content in coastal waters
can override the stress of suboptimal salinity and temperature
(Henrickson et al., 2001). The viruses are even more resistant; they
can survive longer in seawater and can endure better than bacteria
the filtration and purification processes of wastewater treatment
plants (Henrickson et al., 2001; Lipp and Griffin, 2004).
As in most Caribbean countries, only a small part of the popula-
tion in San Andrés is connected to the sewage system, and there is
no previous treatment of the wastewater before its disposal to the
ocean.
Our data show clearly that fecal contamination is worrisome in
several sites of the island, and is above the limits set by law for pri-
mary and secondary contact (Table 2). The situation is critic in
Hooker Bay and in Alcantarillado, where the pathogenic bacteria
are present in high numbers most of the time. Due to its morphol-
ogy, and the quantity of wastewater that directly gets to the bay,
the pollution in Bahía Hooker is even higher than in front of the
sewage system (Alcantarillado). Other sites, in front of beaches
highly popular among tourists, show high values in some occasions
(Tables 2 and 3), evidencing a pollution problem of the coastal
waters of the island, which may pose at risk the swimmers’ health.
The Caribbean Sea is emerging as a marine disease ‘‘hot spot”
(Harvell et al., 1999). Sewage contamination is related to higher
coral mortality (Kaczmarsky et al., 2005). The white pox disease
of the Caribbean coral Acropora palmata is induced by Serratia mar-
cescens, a bacterium of the human intestinal flora (Patterson et al.,
2002).
Some enterovirus are accumulated in coral mucus (Lipp et al.,
2002), even when these pathogens are in concentrations not
detectable in the water, posing at risk, once again, the health of
people and marine ecosystems.
Chaves-Fonnegra et al. (2007), found Escherichia coli in the mu-
cus of the coral Montastraea cavernosa in amounts inversely pro-
portional to the distance from sewage plumes; The
concentrations of E. coli in the mucus were more than 10-fold high-
er than in the Florida Keys. The sponge Cliona delitrix, normally
associated to organic pollution (Ward-Paige et al., 2005; Chaves-
Fonnegra et al., 2007), is abundant at a distance of the raw sewage
discharge (Chaves-Fonnegra et al., 2007).
5. Conclusions
The coastal waters of San Andrés show signs of nutrification,
with nitrogen and phosporous concentrations well above the limit
set for Caribbean non-polluted waters. The presence of contamina-
tion-loving organisms, such as C. delitrix, in great abundance near
the sewage discharge area, together with high concentrations of
pathogenic bacteria, both in the water and in the mucus of stony
corals, should get the attention of the local authorities for a better
management of wastewater. Although there is a common belief
that the pollutants are rapidly diluted in the open waters around
the island, with small or no effect on the coastal ecosystems, evi-
dence from this study and others (e.g. Chaves-Fonnegra et al.,
2007, Mancera et al., in preparation) show that the contaminants,
mainly raw sewage, do have a detrimental effect on the coastal
water quality and the nearby ecosystems, which are the primary
source of income for the island, both for tourism and fishing.
It is therefore urgent to take action for a better management of
the sewage wastewater, both with connecting most population to
the system, and with a treatment plant prior to ocean disposal.
Acknowledgements
We wish to thank Tomàs Guerrero, Project Manager ‘‘Protección
y Manejo sostenible del Recurso Hídrico en el Archipiélago”, from
CORALINA for his support and for allowing us to analyze the data
of CORALINA’s monitoring program. We acknowledge Patricia Ab-
dul, from CORALINA, for providing useful bibliography. We are
grateful to Shennya Ruíz for her help in editing the figures.
This project was co-founded by the research groups Estudios
Ambientales del Caribe, and Modelación de Ecosistemas Costeros
from Universidad Nacional de Colombia.
References
Alongi, D.M., 1998. Coastal Ecosystem Processes. CRC Press LLC, Boca Raton, FL. p.
419.
APHA – AWWA – WPCF, 1995. Standard Methods for Examination of Water and
Waste Water, 19th ed. Washington, D.C.
Bianchi, T., Pennock, J., Twilley, R.R., 1999. Biogeochemistry of Gulf of Mexico
Estuaries. John Wiley and Sons, New York. p. 428.
Bocquené, G., Franco, A., 2005. Pesticide contamination of the coastline of
Martinique. Marine Pollution Bulletin 51, 612–619.
Bruno, J.F., Petes, L.E., Harvell, C.D., Hettinger, A., 2003. Nutrient enrichment can
increase the severity of coral diseases. Ecology Letters 6, 1056–1061.
Burke, L., Maidens, J., 2005. Arrecifes en Peligro en el Caribe. World Resources
Institute, Washington D.C.. p. 84.
Burkholder, J.M., Tomasko, D.A., Touchette, B.W., 2007. Seagrasses and
eutrophication. Journal of Experimental Marine Biology and Ecology 350, 46–72.
Chaves-Fonnegra, A., Zea, S., Gómez, M.L., 2007. Abundance of the excavating
sponge Cliona delitrix in relation to sewage discharge at San Andrés Island, SW
Caribbean, Colombia. Boletín de Investigaciones Marinas y Costeras 36, 63–78.
Cloern, J.E., 1999. The relative importance of light and nutrient limitation of
phytoplankton growth: a simple index of coastal ecosystem sensitivity to
nutrient enrichment. Aquatic Ecology 33, 3–16.
Corredor, J.E., 1976. Aspects of Phytoplankton Dynamics in the Caribbean Sea. FAO
Fisheries Report No. 200, pp. 101–114.
 B. Gavio et al. / Marine Pollution Bulletin 60 (2010) 1018–1030
Corredor, J.E., 1979. Phytoplankton response to low-level nutrient enrichment
through upwelling in the Colombian Caribbean Basin. Deep-Sea Research 26A,
731–741.
Corredor, J.E., Morell, J., Mendez, A., 1984. Dissolved nitrogen, phytoplankton
biomass and island mass effects in the northeastern Caribbean Sea. Caribbean
Journal of Science 20, 129–137.
Corredor, J.E., Howarth, R.W., Twilley, R.R., Morell, J., 1999. Nitrogen cycling and
anthropogenic impact in the tropical interamerican seas. Biogeochemistry 46,
163–178.
Costa Jr., O.S., Nimmo, M., Attril, M.J., 2008. Coastal nutrification in Brazil: a review
of the role of nutrient excess on coral reef demise. Journal of South American
Earth Sciences 257, 270.
Cox, E.F., Ward, Y.S., 2002. Impact of elevated ammonium on reproduction in two
Hawaiian scleractinian corals with different life history patterns. Marine
Pollution Bulletin 44, 1230–1235.
DANE (Departamento Administrativo Nacional de Estadística), 2005. Censo General
2005. Nivel Nacional. Republica de Colombia, p. 50.
Debrot, A.O., Tiel, A.B., Bradshaw, J.E., 1999. Beach debris in Curaçao. Marine
Pollution Bulletin 38, 795–801.
D’Elia, C.F., Wiebe, W.J., 1990. Biogeochemical nutrient cycles in coral-reef
ecosystems. In: Dubinsky, Z. (Ed.), Ecosystems of the World 25 Coral Reefs.
Elsevier, Amsterdam, pp. 49–74.
Diaz, J.M., Garzón-Ferreira, J., Zea, S., 1995. Los Arrecifes coralinos de la isla de San
Andrés, Colombia: Estado actual y perspectivas para su conservación. Academia
Colombiana de Ciencias exactas, físicas y naturales, Colección Jorge Alvarez
Lleras No. 7.
Díaz, J.M., Gómez López, D.I., 2003. Cambios históricos en la distribución y
abundancia de praderas de pastos marinos en la bahía de Cartagena y áreas
aledañas (Colombia). Boletín de Investigaciones Marinas y Costeras 32, 57–74.
Diaz, J.M., Díaz-Pulido, G., Garzón-Ferreira, J., Geister, J., Sanchez, J., Zea, S., 1996.
Atlas de los arrecifes coralinos del Caribe colombiano. I complejos arrecifales
oceánicos. INVEMAR, Santa Marta. p. 29.
Dorfman, M., 2004. Swimming in sewage, the growing problem of sewage pollution
and how the Bush administration is putting our health and environment at risk.
Natural Resources Defense Council and the Environmental Integrity Project 1, 75.
Duarte, C.J., 1995. Submerged aquatic vegetation in relation to different nutrient
regimes. Ophelia 41, 87–112.
Dudgeon, D., 1992. Endangered ecosystems: a review of the conservation status of
tropical Asian rivers. Hydrolobiologia 248, 167–191.
Feller, I.C., 1995. Effects of nutrient enrichment on growth and herbivory of dwarf
red mangrove (Rhizophora mangle). Ecological Monographs 65, 477–505.
Fleisher, J.M., Kav, D., Salmon, R.L., Jonies, F., Wyer, M.D., Godfree, A.F., 1996. Marine
waters contaminated with domestic sewage: nonenteric illnesses associated
with bather exposure in the United Kingdom. American Journal of Public Health
86 (9), 1228–1234.
Fourqurean, J.W., Jones, R.D., Zieman, J.C., 1993. Processes influencing water column
nutrient characteristics and phosphorus limitation of phytoplankton biomass in
Florida Bay, FL, USA: inferences from spatial distributions. Estuarine, Coastal
and Shelf Science 36, 295–314.
Garay, J., Castro, L., 1993. Niveles de hidrocarburos del petróleo en la isla de San
Andrés Caribe colombiano 1992. Boletín Científico CIOH 13, 85–101.
Garay, J., Castillo, F., Andrade, C., Aguilera, J., Niño, L., De La Pava, M., López, W.,
Márquez, G., 1988. Estudio oceanográfico del área insular y oceánica del Caribe
colombiano – archipiélago de San Andrés y Providencia y cayos vecinos. Boletín
Científico CIOH 9, 3–73.
Garay, J., Panizzo, L., Ramirez, G., Lesmes, L., 2001. Anexo 3. Manual de técnicas
analiticas de parametros fisicoquimicos, contaminantes marinos y
microbiologicos en aguas marinas y costeras. In: INVEMAR (Ed.), Diagnostico
y evaluación de la calidad ambiental marina en el Caribe y Pacifico colombiano.
Red de vigilancia para la conservación y protección de las aguas marinas y
costeras de Colombia. Informe técnico final. Tomo I. Santa Marta, pp. 1–74.
Geister, von J., 1975. Riffbau und geologische Entwicklungsgeschichte der Insel San
Andrés (westliches Karibisches Meer, Kolumbien). Stuttgarter Beiträge zur
Naturkunde, Serie B. Nr. 15.
Harborne, A.R., Afzal, D.C., Andrews, M.J., 2001. Honduras: Caribbean coast. Marine
Pollution Bulletin 42 (12), 1221–1235.
Harvell, C.D., Kim, K., Burkholder, J.M., Colwell, R.R., Epstein, P.R., Grimes, D.J.,
Hofmann, E.E., Lipp, E.K., Osterhaus, A.D.M.E., Overstreet, R.M., Porter, J.W.,
Smith, G.W., Vasta, G.R., 1999. Emerging marine diseases-climate links and
anthropogenic factors. Science 285, 1505–1510.
Hatcher, B.G., Johannes, R.E., Robertson, A.I., 1989. Review of research relevant to
the conservation of shallow tropical marine ecosystems. Oceanography Marine
Biology Annual Review 27, 337–414.
Heisler, J., Glibert, P.M., Burkholder, J.M., Anderson, D.M., Cochlan, W., Dennison,
W.C., Dortch, Q., Gobler, C.J., Heil, C.A., Humphries, E., Lewitus, A., Magnien, R.,
Marshallm, H.G., Sellner, K., Stockwell, D.A., Stoecker, D.K., Suddleson, M., 2008.
Eutrophication and harmful algal blooms: a scientific consensus. Harmful Algae
8, 3–13.
Henrickson, S.E., Wong, T., Allen, P., Ford, T., Epsteins, P.R., 2001. Marine swimming-
related illness: implications for monitoring and environmental policy.
Environmental Health Perspectives 109 (7), 645–650.
Herrera, A., Suarez, P., 2005. Indicadores bacterianos como herramienta para medir
la calidad ambiental del agua costera. Asociación Interciencia 30 (003), 171–
176.
Howarth, R.W., 1988. Nutrient limitation of net primary production in marine
ecosystems. Annual Review of Ecology 19, 89–110.
1029
Howarth, R.W., Jensen, H.S., Marino, R., Postma, H., 1995. Transport to and
processing of P in near-shore and oceanic waters. In: Tiessen, H. (Ed.),
Phosphorus in the Global Environment. SCOPE 5:4. Wiley and Sons,
Chichester, pp. 323–345.
Howarth, R.W., Billen, G., Swaney, D., Townsend, A., Jaworski, N., Lajtha, K.,
Downing, J.A., Elmgren, R., Caraco, N., Jordan, T., Berendse, F., Freney, J.,
Kudeyarov, V., Murdoch, P., Zhao-Liang, Z., 1996. Regional nitrogen budgets and
riverine N and P fluxes for the drainages to the North Atlantic Ocean: natural
and human influences. Biogeochemistry 35, 75–139.
Hunter, J.M., Arbona, S.I., 1995. Paradise lost: an introduction to the geography of
water pollution in Puerto Rico. Social Science and Medicine 40 (10), 1331–1355.
IDEAM, 1995. Datos de las variables climáticas de la isla de San Andrés, Providencia
y Santa Catalina. Santafé de Bogotá D.C. Colombia, p. 70.
IGAC, 1986. San Andrés y Providencia: Aspectos geográficos. Instituto Geográfico
Agustín Codazzi. Bogotá D.E., p. 156.
INVEMAR, 2001. Informe del estado de los ambientes marinos y costeros en
Colombia: 2000. Serie Documentos Generales No. 3. Santa Marta, p. 138.
INVEMAR, 2002. Informe del estado de los ambientes marinos y costeros en
Colombia: año 2001. In: Ospina-Salazar, G.H., Acero, A. (Eds.), Medellín: Cuartas
Impresores (Serie de Publicaciones Periódicas/INVEMAR, no. 8), p. 178.
Kaczmarsky, L.T., Draud, M., Williams, E.H., 2005. Is there a relationship between
proximity to sewage effluent and the prevalence of coral disease? Caribbean
Journal of Science 41 (1), 124–137.
Kingsbury, P., 2005. Jamaican tourism and the politics of enjoyment. Geoforum 36,
113–132.
Kjerfve, B., Drude De Lacerda, L., Dias, G.T.M., 2001a. Baia de Guanabara, Rio de
Janeiro, Brazil. In: Seeliger, U., Kjerve, B.J. (Eds.), Coastal Marine Ecosystems of
Latin America. Springer-Verlag, New York. pp. 107–118.
Kjerfve, B., Seeliger, U., Drude De Lacerda, L., 2001b. A summary of natural and
human-induced variables in coastal marine ecosystems of Latin America. In:
Seeliger, U., Kjerve, B.J. (Eds.), Coastal marine ecosystems of Latin America.
Springer-Verlag, New York. pp. 341–354.
Koch, M.S., 1996. Resource availability and abiotic stress effects on Rhizophora
mangle L. (red mangrove) development in south Florida. Ph.D. Dissertation.
University of Miami, Coral Gables, Florida, p. 134.
Kuntz, N.M., Kline, D.I., Sandin, S.A., Rohwer, F., 2005. Pathologies and mortality
rates caused by organic carbon and nutrient stressors in three Caribbean coral
species. Marine Ecology Progress Series 294, 173–180.
Linden, O., 1990. Human impact on tropical coastal zones. Nature Resources 26 (4),
3–11.
Lipp, E.K., Griffin, D.W., 2004. Analysis of coral mucus as an improved medium for
detection of enteric microbes and for determining patterns of sewage
contamination in reef environments. EcoHealth 1, 317–323.
Lipp, E.K., Jarrell, J.L., Griffin, D.W., Lukasik, J., Jacukiewicz, J., Rose, J.B., 2002.
Preliminary evidence for human fecal contamination in corals of the Florida
Keys, USA. Marine Pollution Bulletin 44 (7), 666–670.
Lonin, S., Mendoza, L., 1997. Evaluacion hidrodinámica de las bahías Hooker e
Icacos. Boletín científico CIOH 18, 51–64.
Mancera, J.E., Guerra, L., Ruiz, S.C., Malo, M.A., Pérez, S.P. Evaluación del impacto de
los vertimientos del emisario submarino de San Andrés isla sobre las
comunidades planctónicas a partir de variables fisicoquímicas., in preparation.
Margalef, R., 1965. Composicion y distribucion del fitoplancton. In: Estudios sobre el
Ecosistema Pelagico del N.E. de Venezuela. Memoria de la Fundación La Salle de
Ciencias Naturales 25, 141–208.
Marín, B., 2001. Proyecto Establecimento de valores indicativos del grado de
contaminación de tóxicos químicos y microorganismos de origen fecal, como
base para la expedición de normativas de la calidad de las aguas marinas de
Colombia. COLCIENCIAS. Informe final. Santa Marta.
Marín, B., Cadavid, B., 2001. Descripción general de la calidad de las aguas marinas
de Colombia. Caracterización de la calidad de las aguas marinas. Informe
técnico. Santa Marta, p. 80.
McClanahan, T.R., Sala, E., Stickels, P.A., Cokos, B.A., Baker, A.C., Starger, C.J., Jones IV,
S.H., 2003. Interaction between nutrients and herbivory in controlling algal
communities and coral condition on Glover’s Reef, Belize. Marine Ecology
Progress Series 261, 135–147.
Mignucci-Giannoni, A.A., 1999. Assessment and rehabilitation of wildlife affected by
an oil spill n Puerto Rico. Environmental Pollution 104, 323–333.
Ministerio de Protección Social, Republica de Colombia, 1984. Decreto 1594 de
1984. <http://www.minproteccionsocial.gov.co/VBeContent/library/documents/
DocNewsNo16115DocumentNo4054.PDF> (accessed 22.02.09).
Odum, H.T., Copeland, B.J., McMahan, E., 1972. Coastal Ecosystems of the United
States, vols. 1–4. Conservation Foundation.
Panke, M., Quimby, S., 2000. Pesticides. Caribbean Currents 8 (3), 1–5.
Pastorok, R.A., Bilyard, G.R., 1985. Effects of sewage pollution on coral-reef
communities. Marine Ecology Progress Series 21, 175–189.
Patterson, K.L., Porter, J.W., Ritchie, K.B., Polson, S.W., Mueller, E., Peters, E.C.,
Santavy, D.L., Smith, G.W., 2002. The etiology of white pox, a lethal disease of
the Caribbean elkhorn coral, Acropora palmata. PNAS 99 (13), 8725–8730.
Pennock, J.R., Boyer, J.N., Herrera-Silveira, J.A., Iverson, R.L., Whitledge, T.E.,
Mortazavi, B., Comin, F.A., 1999. Nutrient behavior and phytoplankton
production in Gulf of Mexico Estuaries. In: Bianchi, T., Pennock, J., Twilley, R.
(Eds.), Biogeochemistry of Gulf of Mexico Estuaries. John Wiley and Sons. pp.
109–162.
Peterson, B.J., Frankovich, T.A., Zieman, J.C., 2007. Response of seagrass epiphyte
loading to field manipulations of fertilization, gastropod grazing and leaf
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.,
1998. Review of agricultural pollution in the Caribbean with particular
emphasis on small island developing states. Marine Pollution Bulletin 36 (9),
658–668.
Short, F.T., Davis, M.W., Gibson, R.A., Zimmermann, C.F., 1985. Evidence for
phosphorus limitation in carbonate sediments of the seagrass syringodium
filiforme. Estuarine, Coastal and Shelf Science 20, 419–430.
SIGAM/CORALINA, 2004. Agenda ambiental de San Andrés Islas (on line). <http://
www.coralina.gov.co/archivos/Sigam_CAPITULO%20_I_Perfil_Ambiental_1.pdf>
(Fecha de consulta 29/10/2007).
Siung-Chang, A., 1997. A review of marine pollution issues in the Caribbean.
Environmental Geochemistry and Health 19, 45–55.
Steer, R., Arias, F.A., Ramos, A., Sierra, P.C., Alonso, D.A., Ocampo, P., 1997.
Documento base para la elaboración de la política nacional de ordenamiento
integrado de las zonas costeras. Documento de consultoría. INVEMAR. Serie
Publicaciones Especiales 6, 395.
Twilley, R.R., 1995. Properties of mangrove ecosystems related to the energy signature
of coastal environments. In: Hall, C.A.S. (Ed.), Maximum Power: The Ideas and
Applications of H.T. Odum. University Press of Colorado, Niwot, CO, pp. 43–62.
Twilley, R.R., Cowan, J., Miller-Way, T., Montagna, P., Mortazavi, B., 1999. Benthic
fluxes of selected estuaries in the Gulf of Mexico. In: Bianchi, T., Pennock, J.,
Twilley, R. (Eds.), Biogeochemistry of Gulf of Mexico Estuaries. John Wiley and
Sons. pp. 163–209.
Twilley, R.R., Cárdenas, W., Rivera-Monroy, V.H., Espinoza, J., Suescum, R., Armijos,
M.M., Solórzano, L., 2001. Ecology of the Gulf of Guayaquil and the Guayas River
Estuary. In: Seeliger, U., Kjerve, B.J. (Eds.), Coastal Marine Ecosystems of Latin
America. Springer-Verlag, New York, p. 360 (pp. 245–263).
Vitousek, P.M., Howarth, R.W., 1991. Nitrogen limitation on land and in the sea:
how can it occur? Biogeochemistry 13, 87–115.
Ward-Paige, C.A., Risk, M.J., Sherwood, O.A., Jaap, W.C., 2005. Clionid sponge surveys
on the Florida Reef Tract suggest land-based nutrient inputs. Marine Pollution
Bulletin 51, 570–579.