Marine Pollution Bulletin 120 (2017) 379–386

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Marine Pollution Bulletin

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Baseline

Polycyclic aromatic hydrocarbons and heavy metals in the Cispata Bay, MARK
Colombia: A marine tropical ecosystem
Saudith Burgos-Núñeza,⁎, Amado Navarro-Frómetab, José Marrugo-Negretea,
Germán Enamorado-Montesa, Iván Urango-Cárdenasa
a
Water, Applied and Environmental Chemistry Group, Department of Chemistry, Faculty of Basic Sciences, University of Cordoba, Montería, Colombia
b
Food and Environmental Technology Department, Technological University of Izucar de Matamoros, Izucar de Matamoros, Mexico

A R T I C L E I N F O A B S T R A C T

Keywords: The concentrations of polycyclic aromatic hydrocarbons and heavy metals were evaluated in shallow sediments,
Cispata Bay water, fish and seabird samples from the Cispata Bay, Colombia. The heavy metals concentrations in the
Heavy metals sediment was in the following order: Cu > Pb > Hg > Cd. The heavy metal concentration was different
Marine pollution (p < 0.05) in juvenile and adult birds. High concentrations of mercury were registered in the seabird
Polycyclic aromatic hydrocarbons
(10.19 ± 4.99 mg kg− 1) and fish (0.67 μg g− 1) samples. The total concentration of polycyclic aromatic
Seabird
Seafish
hydrocarbons ranged from 7.0–41 ng g− 1 in sediment, 0.03–0.34 ng mL− 1 in water samples, 53.24 ng g− 1 in
fish, and 66 ng g− 1 in seabirds. The high concentrations of heavy metals in seabirds may be explained by their
feeding habits. The presence of polycyclic aromatic hydrocarbons in the Cispata Bay may be due to hydrocarbon
spills during oil transport at the nearby oil port.

Since industrialization during the 1940s–1950s, the amount of toxic
substances and pollutants entering a variety of environmental ecosys-
tems has increased. In marine and coastal ecosystems, the levels of
these compounds are high due to pollutant inputs from rivers and
streams and atmospheric deposition (Burger and Gochfeld, 2004,
2009). These pollutants include organic and inorganic compounds,
such as polycyclic aromatic hydrocarbons (PAH) and heavy metals
(HM), respectively (US EPA, 2006). Additionally, the oil industry is
responsible for releasing wastes such as PAH, olefinic and aliphatic
hydrocarbons, HM, nitrogen and sulfur compounds to the environment
(Abdollahi et al., 2013).
PAH have two or more aromatic rings in linear or angular
arrangements. In addition, they can be categorized according their
molecular weight as high molecular weight polycyclic aromatic hydro-
carbons (HMW-PAH) and low molecular weight polycyclic aromatic
hydrocarbons (LMW-PAH) (Abdollahi et al., 2013). These compounds
are derived from natural sources as well as from anthropic activities,
e.g., the burning of fossil fuels and coal (Kannan and Perrotta, 2008). In
this sense, chronic or accidental oil spills and fuel extraction activities
represent a significant source of PAH pollution, which threatens marine
biota. In fact, numerous studies assessing the impacts of PAH have been
performed on marine ecosystems affected by oil spills or coastal zones
near heavily industrialized regions (Roscales et al., 2011). The most
recent works highlight that even slight/low/minor concentrations of
some PAH and HM in seawater/saltwater can elicit harmful effects on
aquatic organisms (Oliva et al., 2012). Indeed, in fish, these compo-
nents are transformed into carcinogenic and mutagenic compounds,
leading to hepatic injury, altered gonadal development and the onset of
tumours (Abdollahi et al., 2013).
Heavy metals (HM) encompass a wide range of non-degradable
substances able to accumulate in tissues of different living organisms
(Jakimska et al., 2011; Oliva et al., 2012). HM enters the aquatic
environment from industrial dumping, urban wastewater, atmospheric
precipitations and urban stormwater runoff (Naser, 2013). Addition-
ally, metals may be associated with particulate material and favour its
entry into the marine environment (Haynes and Johnson, 2000).
Another entry route of HM into marine environments includes the
atmospheric transport of soil dust and sediments through terrestrial
fluxes and fluvial ways. Though some heavy metals are classified as
essential for normal physiological processes, high concentrations have
deleterious effects on human health and biota. In addition, the use of
cadmium (Cd), copper (Cu), mercury (Hg) and zinc (Zn) is widely
allowed in agricultural activities. Fertilizers containing small fractions
of Zn and Cu are used to incorporate these elements into deficient soils,
whereas arsenic (As), Cd and Hg are components of some fungicides.
Additionally, Cu is employed as algaecide, while Cd and Zn may be
present in phosphate fertilizers (Haynes and Johnson, 2000; Nacke
et al., 2013). Furthermore, all of these species promote a range of toxic

⁎
Corresponding author at: Department of Chemistry, University of Cordoba, Cra 6 # 76-103, Monteria, Colombia.
E-mail address: smburgos@correo.unicordoba.edu.co (S. Burgos-Núñez).

http://dx.doi.org/10.1016/j.marpolbul.2017.05.016
Received 29 December 2016; Received in revised form 4 May 2017; Accepted 8 May 2017
Available online 12 May 2017
0025-326X/ © 2017 Elsevier Ltd. All rights reserved.
S. Burgos-Núñez et al.
effects in polluted aquatic environments (Radic et al., 2013). Despite
this, little attention has been given to the behaviour of these pollutants
in the seabirds from tropical ecosystems, although recent studies have
linked the detection of HM in animal tissues with the presence of these
metals in sediments (Abbasi et al., 2015).
In terms of biodiversity, the Cispata Bay in Colombia represents a
highly productive ecosystem, which encloses one of the largest
mangrove areas in the region and harbours many birds from the Sinu
River Delta. However, recent findings appear to indicate that this zone
has been affected by chemical fertilizer runoff, herbicides, pesticides,
domestic wastewater inflow and spills of harmful substances such as
hydrocarbons and HM. Feria et al. (2010) and Paternina-Uribe (2011)
note that high concentrations of HM in the Bajo Sinu region follow the
overuse of fertilizers and dumping in the La Doctrina irrigation district.
Additionally, it is worth noting that phosphate fertilizers, such as
superphosphate, which are widely used in this region, have high
concentrations of Cr, Cu, Ni, Pb, and Zn, while calcium-based fertilizers
have high concentration of Pb and Zn. Subsequently, the fate of these
overcharged waters ends in Cispata Bay. The current study assesses
sixteen PAH and HM in samples of sediment, water, fish and seabirds
from the Cispata Bay, Colombia, to evaluate the impact of anthropic
activities and to build a solid knowledgebase to make decisions and
implement a legal framework around the management of these
substances.
Cispata Bay is located in the Colombian Caribbean Coast, Cordoba
province, between 09°25′12″–09°20′8″N and 75°47′37″–75°55′30″W
(Sánchez et al., 2005). The bay is surrounded by a dense mangrove
forest and has a tropical climate, where approximately 400 families live
on fishing (fish, oysters, mussels and snails) and wood production
(Sánchez-Páez et al., 1997). At present, the bay is surrounded by areas
with intensive agriculture and a large variety of commercial fishing
activities (shrimp and tilapia farming). Additionally, it is important to
emphasize that the tourism sector has experienced rapid growth in the
area. An oil port is located approximately 12 km from the Cispata Bay.
The non-biological samples, water and sediments, were collected from
the followed sites: Terraplen (S1), Zarapa (S2), near the port (S3), the
Pila (S4), Mogotes (S5). All sample points are marked in Fig. 1.
All surface sediment samples were collected with a Van Veen-type
grab sampler. To analyse the metal content, sediment subsamples were
taken with plastic spoons from the middle part of the dredge at a depth
no > 5 cm and transferred to 250 mL polypropylene flasks. To analyse
the PAH content, sediment subsamples were taken with a stainless steel
spoon, and transferred to amber glass bottles. All sediment samples
were refrigerated until laboratory analysis. For water sampling, a Van
Dorn horizontal bottom sampling bottle was used, and 1 L subsamples
were taken and stored in polyethylene bottles and preserved with HNO3
at pH 2.0 for heavy metal analysis and amber glass bottles for PAH
analysis. All water samples were refrigerated at 4 °C until laboratory
analysis (APHA, 2005). Biological samples were collected from seafish
with the help of local fishers in the estuary by employing nets. Collected
specimens were Cetengraulis edentulus (n = 7), Eugerres plumieri
(n = 6), Centropomus undecimalis (n = 5) and Trichirus lepturus
(n = 5). The samples were stored in plastic bags for HM analysis and
aluminium foil for PAH analysis. The resident birds studied were
Pelecanus occidentalis (n = 11) and Fregata magnificens (n = 7), and
the migratory birds studied were Phalacrocorax brasilianus (n = 10) and
Thalasseus maximus (n = 5). The samples were collected between
March and June 2010, and February 2011, from the Cispata Bay. The
total concentrations of Hg, Cu, Pb, Cd and Zn in blood and feathers
were determined, while the PAH concentrations were evaluated in only
the blood of the collected birds. The birds were caught near the fishing
boats following all ethical procedures, and the feather and blood
samples were subsequently obtained. The feathers were stored in plastic
bags, and blood was stored in heparinized tubes and refrigerated until
analysis. HM analysis of the sediment samples was performed using
lyophilized samples. The feather samples were washed with deionized
380
Marine Pollution Bulletin 120 (2017) 379–386
water and acetone and packed in polypropylene-free metal bags. The
feathers were dried for 24 h in an oven at 60 °C, and the dry weight was
obtained. For mercury analysis, 30–40 mg of the sediment sample was
digested with H2SO4-HNO3 (2:1) at 100–110 °C for 3 h and KMnO4
solution (5%) at 100 °C for 30 min. The total mercury analysis was
performed by cold-vapor atomic absorption spectroscopy (CVAAS) at a
wavelength of 253.7 nm using an ICE 3000 spectrophotometer (Thermo
Electron Corporation, Alemania) (Marrugo-Negrete et al., 2008). Cd,
Pb, Zn and Cu analyses were performed on 0.4–0.5 g of the sediment
sample treated with a mixture of HNO3-H2O2 (7:3) and heated for
45 min. The digested sample was filtered and filled to 25 mL with Milli-
Q water. The measurements of the digested samples were performed
using an ICE 3000 spectrophotometer (Thermo Electron Corporation,
Alemania) (Dauwe et al., 2003). Quality control was performed using
the certified reference material IAEA-086 (methylmercury, total mer-
cury and other trace elements in human hair), IAEA-A-13 (trace
elements in freeze dried animal blood), DORM-2 (dogfish muscle for
trace metals), SRM 1641d (mercury in water) and SRM 1641e (trace
metals in water), and the percentages of recovery achieved values up to
90% in all cases. Another quality control parameters and limit of
detection are shown in Appendix A.
For the analysis of PAH in sediments, 15 g of the sample was mixed
with anhydrous Na2SO4 and sonicated three times with 40 mL of n-
hexane. The extract was passed through a column containing anhydrous
Na2SO4 and glass wool (US EPA, 2007). Finally, the extract was
concentrated by rotary evaporation. Water samples were analysed
according to EPA method 3510c (US EPA, 1996). Fish samples were
treated with methanolic KOH and refluxed for 4 h. The hydrocarbon
concentrate was obtained by extraction of the liquid with hexane, and
the concentration and extraction in the solid phase was performed with
C18 cartridges. Blood samples from birds were centrifuged (3000 rpm
for 10 min). The obtained plasma was mixed with 10 mL of methanol to
denature the plasma proteins, sonicated and extracted three times with
20 mL of dichloromethane. The combined extracts were passed through
a C18 cartridge with a layer of anhydrous Na2SO4, and finally, the
extract volume was reduced to 2 mL by rotary evaporation (Naufal,
2008). The extracts were performed by gas chromatography coupled to
mass spectrometry (GC–MS) using a Trace GC Ultra® chromatograph
system with a DSQ II quadrupole mass spectrometer (Thermo Electron
Corporation). A DB-5MS capillary column (5% diphenyl/95% dimethyl-
polysiloxane, 30 m × 0.25 mm i.d. × 0.25 μm) from Restek was em-
ployed. The carrier gas was helium at a flow rate of 1 mL min− 1. The
mass spectrometer was operated in electronic impact mode (70 eV),
maintaining the chromatograph interphase and source temperature at
280 °C. Ion monitoring started after 2.5 min. The injection temperature
was 290 °C, and the injection volume was 2 μL in splitless mode. The
temperature program was set as follows: 80 °C for 1 min, 4 °C min− 1 up
to 280 °C for 9 min. The PAH concentrations were determined with a
calibration curve of the 16 priority contaminants: fluorene (Fl),
phenanthrene (Phen), anthracene (Ant), fluoranthene (Flt), pyrene
(Pyr), benz[a]anthracene (BaA), naphthalene (Naph), benzo[b]fluor-
anthene (BbF), indeno[1,2,3-cd]pyrene (Ind), benzo[ghi]perylene
(BghiP), chrysene (Chry), acenaphthylene (Acnaphtil), acenaphthene
(Acnphta), benzo[k]fluoranthene (BkF), benzo[a]pyrene (Bap) and
dibenz[a,h]anthracene (DiBahA). A not normal distribution (Bartlett
test) was follow by HM and PAH levels in all the matrices evaluated;
therefore, nonparametric statistics were used for comparisons. The
Kruskal Wallis test was used to test for significant differences between
species and age (juvenile/adults) of the birds. When significant
differences were found, Mann-Whitney multiple-rank tests were con-
ducted (Burger and Gochfeld, 2004; Burger, 2008). To determine the
sources of PAH, some well-known indices were calculated: LMW-PAH/
HMW-PAH, carbon preference index (CPI), pristane/phytane (Pr/Phy),
pristane/nC17 (Pr/nC17), and phytane/nC18 (Phy/nC18) (Zaghden et al.,
2007). Additionally, to identify the sources of these compounds,
correlations between the content of HM and PAH in fish and birds
S. Burgos-Núñez et al. Marine Pollution Bulletin 120 (2017) 379–386

Fig. 1. Study area: Cispata Bay, Cordoba, Colombia.

were examined. The limit of detection and quality control parameters
are detailed in Appendix A.
The results showed that at least one PAH was detected in all of the
water, sediment, fish muscle and bird blood samples, as shown in
Table 1. The higher concentration was registered at area S1. It should
be noted that at this location, the concentrations of both LMW-PAH
(naphthalene, acenaphthene) and HMW-PAH (indeno[1,2,3-cd]pyrene
and dibenz[a,h]anthracene) were markedly increased. Similarly,
Dhananjayan et al. (2012) reported concentrations ranging between
8.66 and 46.74 μg L− 1 in oceanic water from Mumbai from sampling
points near refineries and petrochemical plants. Similarly, Kafilzadeh
(2015) reported the existence of PAH (47.3 and 385 μg L− 1) in waters
from the Soltan Abad River, which runs through the city of Shiraz,
which is well known for its poor air quality due to industrial growth
(Gharehchahi et al., 2013; Farzadkia et al., 2014). On the other hand,
the LMW-PAH/HMW-PAH index was superior to that of sampled
sediments near the port area (S1 and S3, respectively), as shown in
Table 1. These results can be attributed to petrogenic sources due to

Table 1
Concentration of polycyclic aromatic hydrocarbons (PAH) in seabird blood (ng mL− 1), fish muscle (ng g− 1), water (μg L− 1) and sediment (ng g− 1) from the Cispata Bay.

Sample Naph Acnaphtil Acnphta Fl Phen Ant Flt Pyr BaA Chry BbF BkF Bap Ind DiBahA BghiP TPAH LMW/HMW

Birds 26.91 1.43 4.75 2.71 15.24 ND 5.40 3.96 0.19 0.39 1.36 ND 0.33 ND 2.63 0.50 65.81 3.63
Fish 3.06 1.40 3.31 4.12 16.37 ND 5.29 4.02 0.06 ND 0.01 ND 0.38 0.92 12.39 1.80 53.14 1.29
W1 25.47 5.19 83.19 2.96 15.92 ND 5.82 3.83 1.91 3.34 21.38 ND 5.03 34.61 115.83 20.32 344.78 0.63
W2 12.46 4.96 8.96 5.15 10.47 ND 3.66 1.01 ND ND ND ND ND 7.84 40.10 4.65 99.26 0.73
W3 0.94 2.26 7.90 4.03 8.40 ND 3.44 1.75 0.12 0.95 1.15 ND ND 4.87 31.70 7.66 75.18 0.46
W4 0.80 2.09 5.77 0.27 2.81 ND 2.48 0.03 ND ND ND ND ND ND 12.93 1.97 29.15 0.67
W5 0.19 1.92 5.54 0.20 0.92 ND 2.16 ND ND ND ND ND ND ND 14.94 1.86 27.74 0.46
S1 1.51 0.09 0.49 0.80 2.85 ND 0.33 0.28 ND 0.15 0.01 ND ND ND 0.18 0.03 6.71 5.84
S2 0.46 0.05 0.22 0.25 1.01 ND 0.61 0.72 0.79 0.95 1.47 0.05 22.20 0.83 0.47 0.38 30.47 0.07
S3 2.56 0.15 1.12 2.02 8.44 ND 1.18 1.77 ND 0.58 0.17 0.05 1.09 0.05 0.18 0.08 19.44 2.77
S4 0.82 0.06 0.51 0.58 5.49 ND 5.01 4.74 2.32 3.04 8.32 0.56 4.17 2.26 0.71 2.38 40.98 0.22
S5 0.27 0.04 0.12 0.14 0.80 ND 0.25 0.39 0.02 0.40 0.47 ND 6.15 0.15 0.68 0.10 9.97 0.16

The LMW-PAH/HMW-PAH ratio corresponds to ∑ Naph + Aceph + Ace + Fl + Fe + Ant/∑Flt + Pir + BaA + Cri + BbF + BkF + Bap + Inp + DiBahA + BghiP.
ND: not detected.

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S. Burgos-Núñez et al.
crude oil transportation at the port. However, the highest total
concentration of PAH found in sediments (in the current study,
40 ng g− 1) was lower than that reported by Veiga et al. (2009)
(131.3–948.1 ng g− 1) in affected areas from the Galicia coast following
the Prestige oil spill. Likewise, our findings were also lower than those
reported by Johnson-Restrepo et al. (2008) and Parga-Lozano et al.
(2002) at La Caimanera swamp (234 ng g− 1) and Cartagena Bay
(1415 μg g− 1), respectively. Nevertheless, the concentrations in our
study were similar to those obtained by Medeiros et al. (2005) at the
Patos Lagoon estuary, Brazil (37.7–11,800 ng g− 1), where there is
intense petrochemical activity, marine transport and sewage. As pre-
viously mentioned, the occurrence of PAH in the studied area repre-
sents a threat to the whole Cispata Bay ecosystem because of the
frequent spills. In addition, the total concentrations of PAH and HMW-
PAH in the current study were lower than the effects range low (ERL)
concentration proposed by the National Oceanic and Atmospheric
Administration (NOOA) in their Screening Quick Reference Tables
(SQUIRTs) for organic compounds in marine sediments. According to
Baumard et al. (1998), concentrations of PAH found in sediments from
Cispata Bay can be considered as low levels of contamination
(0–100 ng g− 1). The CPI, Pr/Phy, Pr/nC17 and Phy/nC18 indices are
shown in Table 2. The carbon preference index (CPI) was more than
two in all sampled sediments, revealing a contribution of biogenic
paraffins in all samples that could be explained by the proximity to the
mangrove. On the other hand, isoprenoids, such as phytane (2,6,10,14-
tetramethylhexadecane) and pristane (2,6,10,14-tetramethylpentade-
cane), were also detected, suggesting the influence of petrogenic
sources (Blanco et al., 2006). The Pr/Phy ratio ranged between 1.16
(S4) and 2.04 (S5), indicating a biogenic contribution as a result of
phytol degradation by zooplankton, which agrees with the CPI result.
Moreover, minor biodegradation of hydrocarbons in the samples was
observed, as the Pr/n-C17 and Phy/n-C18 ratios were lower than one. In
other words, n-alkanes are progressively depleted in oil samples when
the degree of weathering increases; thus, it can be stated that the
greater resistance to degradation of the isoprenoids leads to an index
higher than one, which demonstrates the presence of hydrocarbons
(Companioni-Damas et al., 2011; Wang et al., 2013). To determine the
origin of the PAH found in sediments from the Cispata Bay, we used the
m/z 85 common fragment ion for n-alkanes. The chromatographic
profiles of the sediments (Fig. 2) showed similar tendencies for
sediments collected near the port (S1, S3 and S4) and at sampling
points away from the port (S2 and S5). Additionally, the chromato-
grams also display the m/z 125 fragment, corresponding to one
unresolved complex mixture (UCM) in the former group (sampling
points nearest the port), which is indicative of the presence of
petroleum hydrocarbons (Tolosa et al., 2004; Abdallah et al., 2015).
However, a lower proportion of UCM was also observed in the latter
group (sampling points away from the port), suggesting contamination
to a lesser extent. On the other hand, PAH concentrations found in fish
tissues were similar to those of Cheung et al. (2007), showing a
15.5–118 ng g− 1 wet weight. Likewise, the LMW-PAH/HMW-PAH
index was higher than one, indicating the presence of petrogenic
hydrocarbons in the assessed fish tissues. In addition, the PAH
composition in the assessed fish muscles was widely dominated by
molecules with two, three, and four rings, which are associated with
Table 2
Biomarker indices used to establish the pollution sources in sediments from Cispata Bay.
Indices S1 S2 S3 S4
CPI 2.34 2.40 1.93 1.92
Pr/Phy 1.21 1.90 2.46 1.16
Pr/nC17 0.33 0.26 0.44 0.26
Phy/nC18 0.77 0.51 0.55 0.73
CPI: carbon preference index; Pr: pristane; Phy: phytane.
Marine Pollution Bulletin 120 (2017) 379–386
petrogenic contamination (Cheung et al., 2007). Several compounds
derived from petrogenic activity were observed in the assessed samples.
In this respect, naphthalene was present in all samples, probably
because of its high solubility.
A high concentration of phenanthrene was also found in the fish
samples. Considering this evidence, this finding could explain the high
concentration found in the sampled birds. It is well known that several
filter feeder fishes are able to absorb large volumes of water, and thus,
fish are prone to bioaccumulate xenobiotics through their gills and
gastrointestinal tract. In polluted aquatic environments, fish are
exposed to both dissolved and particulate fractions of hydrocarbons
existing in the water column, but the proportion will depend on the
solubility. Therefore, fish might absorb low molecular weight PAH
directly from water, whereas high molecular weight PAH can be
obtained through the intake of particulate material within the gastro-
intestinal tract (Yap et al., 2012).
Although the sediment samples showed concentrations below those
reported at polluted areas, several fish displayed BaP levels above the
maximum level recommended for safe consumption (EPD, 1993: US
EPA, 2000). This fact is alarming since spills increase the risk of
contamination and transmission through the food chain. Indeed, fish
consumption is high for people living around this area, which in turn
increases the exposure level to these harmful substances. Mean
concentrations of naphthalene and fluoranthene (26.0 and
6.0 ng mL− 1, respectively) were detected in all bird blood samples.
Similarly, fluorene (4 ng mL− 1), phenanthrene (4 ng mL− 1) and pyr-
ene (4 ng mL− 1) were detected in 83% of the samples analysed,
whereas mean concentrations of acenaphthene, fluoranthene and
chrysene were found in 33% of the samples (2.0, 6.0 and 2.0 ng mL− 1,
respectively). Moreover, the mean total PAH concentration was
66.0 ng mL− 1. In this regard, Troisi et al. (2007) reported slightly
higher mean PAH values (10.0 to 180 ng mL− 1) in blood samples from
Common Murre, Uria aalge, from the Wash Norfolk Coast, England,
after unidentified local spills. It should be noted that some PAH extend
their durability within the body of vertebrates through enterohepatic
circulation (Perez et al., 2008). The LMW-PAH/HMW-PAH ratio was
higher than one, demonstrating that petrogenic activity is the origin of
these pollutant sources (Yap et al., 2012), which could be attributed to
Coveñas port. Similarly, Perez et al. (2008) found that PAH profiles in
blood samples of seagulls was dominated by naphthalene (22–38%)
from petrogenic origin, attributed to the Prestige oil spill. Generally,
PAH from petrogenic origin are absorbed more readily than those of
pyrogenic origin because they can strongly bind to particulate material.
Heavy metals were not detected at any water sampling points in this
study. Meanwhile, high concentrations of HM were found in sediments
from the S2 and S5 sampling points, located near the mangrove areas
(see Table 3). We considered two explanations for this observation: on
one hand, the anoxic conditions of this ecosystem could promote the
resuspension of HM in the water column, leading to the high levels
observed, while on the other hand, mangrove areas promote the
deposition of fine particles with a high content of minerals and organic
material enriched with metals. Thereby, this ecosystem represents a
good scenario to understand several processes involved in the hydro-
geochemical dynamic of this environment, such as mixing, dissolution,
evaporation and chemical exchange of HM between water and sediment
(Ramanathan et al., 1999; Bodin et al., 2013). The HM concentrations
were observed in the order of Cu > Pb > Hg > Cd. Although the Hg
level was unaccountably lower than that of Pb and Cu, Paternina-Uribe
(2011) noted that Hg showed a higher bioavailability than the other
S5 assessed metals in the study area. The concentration of metals in
sediments may be influenced by several factors, including the degree to
2.47 which sediments are able to join or release pollutants. Moreover, the
2.04
pH, cationic exchange capacity, organic matter content, redox poten-
0.51
0.42 tial, chloride content and salinity also determine the absorption degree,
mobility, bioavailability and toxicity of metals. According to Paternina-
Uribe (2011), these factors influence the concentrations of metals in
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Fig. 2. a. Unresolved compound mixture from sediment samples from Cispata Bay. b. Typical composition distributions of n-alkanes, as n-C13 to n-C34 were detected in sediments samples
from the Cispata Bay. Pr: Pristane; Phy: Phytane.

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S. Burgos-Núñez et al. Marine Pollution Bulletin 120 (2017) 379–386

Table 3 2011). We wish to highlight that in the current study, the Hg levels
Heavy metal concentrations in sediments from Cispata Bay. found in birds were higher than 5.0 mg kg− 1 for the P. occidentalis and
F. magnificens specimens (5.151 and 10.192 mg kg− 1, respectively). It
μg Cd g− 1 μg Pb g− 1 μg Cu g− 1 ng Hg g− 1
is possible that seabirds can tolerate high concentrations of Hg due to
S1 < lc 0.51 1.63 1.63 their ability to demethylate mercury in the liver and subsequently store
S2 0.009 0.87 12.93 12.93 it in the form of inorganic Hg (Burger and Gochfeld, 2001).
S3 < lc 0.49 5.99 5.99
In addition, an increased concentration of Pb was observed in P.
S4 0.014 0.70 2.36 2.36
S5 < lc 1.39 15.36 135.66 brasilianus specimens; however, this Pb level is lower than that reported
by Tsipoura et al. (2011) and does not represent a threat to the assessed
birds since only Pb levels above a certain threshold (4 mg g− 1) are
Table 4 considered unsafe. Lead is one of the most studied metals in seabirds as
Heavy metal concentrations (μg g− 1) in fish from Cispata Bay. a consequence of the release of this metal into the atmosphere by
industrial and vehicular activities (Ruelas-Inzunza and Paez-Osuna,
Seafish species Hg Cd Pb Cu
2004). Since a significant Pb body load is accumulated in feathers, there
Cetengraulis edentulus 0.10 0.004 0.08 0.45 is a positive correlation between the Pb concentration in feathers and
Eugerres plumieri 0.14 < lc 0.04 0.16 Pb accumulation in internal tissues; hence, feathers are good indicators
Centropomus undecimalis 0.38 0.010 0.04 0.23 of lead contamination in marine environments (Burger, 1993). The Cd
Trichirus lepturus 0.67 < lc 0.12 0.33
concentrations found in P. occidentalis (0.40 μg g− 1) were higher than
those reported by Ruelas-Inzunza and Paez-Osuna (2004) and Bond and
sediments from the Cispata Bay. For water samples, the concentrations Lavers (2011) of 0.1 μg g− 1 and 0.29 μg g− 1, respectively. Generally,
of HM show a similar pattern as that observed in the sediments. Cd concentrations in birds are higher in the kidney than the liver and
Additionally, the presence of these pollutants in the Cispata Bay muscle, and consequently, Cd levels are lower in the feathers (Guillén
sediments could also be related to sewage discharge rich in organic et al., 2010). Likewise, the Cd concentration reflects the levels of HM in
matter from neighbouring towns favouring metal accumulation. In blood during feather development (Dauwe et al., 2003). In general,
addition, Cispata Bay is irrigated by a fluvial network encompassing almost 30% of the Cd body load of birds can be found on the feathers,
swamps and the Sinu River, which in turn carries pollutants from farm and this value is lower than that of the Hg and Pb values. Though the Cd
activities (Paternina-Uribe, 2011). The concentrations of HM in fish concentration in feathers is usually low, it should not be neglected that
muscle were observed in the order of Hg > Cu > Pb > Cd (see this concentration can be of endogenous origin (Bond and Lavers,
Table 4). Nonetheless, our outcomes were lower than those of Yi et al. 2011). Concentrations of heavy metal were significantly different
(2011): Cu, 0.361–18.76 mg kg− 1; Pb, 0.009–10.1 mg kg− 1; and Cd, (p < 0.05) between juvenile and adult birds, suggesting that metal
ND–2.0 mg kg− 1; except for that of Hg, ND–0.054 mg kg− 1. Recently, accumulation depends on the exposure time. In contrast, the accumula-
Paternina-Uribe (2011) reported the presence of HM in fish from tion levels of HM for the migratory seabird Thalasseus maximus showed
Cispata Bay and also found a high bioavailability of Hg around the a different pattern, possibly as a result of different exposure levels to
study area. It is well accepted that fish consumption elicits several HM from the different places that these birds inhabit during their life
beneficial effects on human health due to its content of polyunsaturated cycle. In addition, HM concentrations may be influenced by the feeding
fatty acids (n − 3, n −6), protein, vitamins and minerals. and metabolism of the assessed organisms (Pérez et al., 2005). As
The concentrations of HM in bird feathers were found in the order of Zamani-Ahmadmahmoodi et al. (2009) noted, concentrations of Hg in
Zn > Cu > Hg > Pb > Cd (see Table 5). An increased concentra- birds reflect the local contamination by Hg, while the Hg load from
tion of Cu was observed in Pelecanus occidentalis, whereas a relatively migratory birds reflects the food diversity from a wide geographical
high concentration of Zn (78.96 mg kg− 1) was observed in Fregata region. The concentrations of Pb, Cu, and Hg in feathers are correlated
magnificens. It is noteworthy that our findings differed from those of with the bill length, wing length and weight of the assessed organism,
Pérez et al. (2005), because the Zn and Cu concentrations in birds from indicating that these pollutants increase with the age of the organism.
Cispata Bay are higher than those found in seabirds from the Galicia From of our view, seabirds can obtain different loads of pollutants
coast, whose Zn and Cu concentrations were 12.54 and 0.81 mg kg− 1, through feeding, which could explain the levels observed here.
respectively. According to the same authors, Zn and Cu are metaboli- Additionally, the main entry route of these pollutants into wild animals
cally regulated in the tissues of birds, which could explain the high is through food, which consequently, depending on the nature of the
levels observed. Regarding the Hg levels, significant differences contaminant, indicates the concentration from different trophic levels
(p < 0.05) were noted between Pelecanus occidentalis and Phalacrocor- (Ruelas-Inzunza and Paez-Osuna, 2004). There was no detected Cd
ax brasilianus. As noted by Lucia et al. (2010), bird feathers provide an concentration in the blood of the assessed specimens. The Pb concen-
excretion route for excess metals such as Hg, since this metal can tration in the blood of P. occidentalis (1127.96 μg L− 1) in the current
accumulate in feathers due to its affinity for sulfhydryl groups in the study was greater than that in the blood of Audouin's gull Larus
keratin. Recent evidence appears to indicate that an Hg concentration audouinii from the Island of Isla Grosa, Murcia, Spain, whose Pb
above 5.0 mg g− 1 impairs reproductive performance (Tsipoura et al., concentration was 719 μg L− 1 (García et al., 2005). Note that Pb is

Table 5
Heavy metal concentrations in the feathers of birds from Cispata Bay.

Age Bird species mg Cd kg− 1 mg Pb kg− 1 mg Cu kg− 1 mg Hg kg− 1 mg Zn kg− 1

Juvenile P. occidentalis 0.009 ± 0.01 0.50 ± 0.67 1.76 ± 1.61 1.77 ± 0.71 23.31 ± 14.16
P. brasilianus < LD 0.15 ± 0.32 19.90 ± 18.14 1.76 ± 0.65 14.19 ± 2.55
F. magnificens 0.34 ± 0.32 0.19 ± 0.09 3.65 ± 4.99 2.10 ± 1.36 61.64 ± 42.39
T. maximus 0.16 ± 0.21 0.08 ± 0.02 0.35 ± 0.60 0.96 ± 0.46 19.33 ± 11.75
Adults P. occidentalis 2.01 ± 2.84 0.68 ± 0.25 86.84 ± 131.11 5.15 ± 1.52 21.88 ± 11.68
P. brasilianus < LD 0.69 ± 0.06 51.31 ± 3.23 4.99 ± 1.47 22.13 ± 3.28
F. magnificens 0.36 ± 0.23 0.51 ± 0.27 13.42 ± 26.23 10.19 ± 4.99 78.96 ± 37.55
T. maximus 2.43 ± 0.59 0.04 ± 0.31 45.22 ± 60.27 3.57 ± 1.37 27.39 ± 12.48

384
S. Burgos-Núñez et al.
Fig. 3. Variation of the heavy metal concentrations in sediments, fish and seabirds from the Cispata Bay.
widely used as an anti-corrosive compound for ship painting and as an
antiknock agent of gasoline and diesel fuels (Abdollahi et al., 2013).
The Hg concentrations were registered between 0.23 and 1.09 μg L− 1
with the greater level found in P. occidentalis. It is noteworthy that
blood provides a direct fingerprint of the dietary exposure to Hg
(Hargreaves et al., 2011).
The bioaccumulation of HM and PAH in marine organisms was also
evaluated in this study. As shown in Fig. 3, the Hg and Cd concentra-
tions indicate bioaccumulation in the Cispata Bay ecosystem, as the
concentrations of these metals increase with the food chain level in
environments with very low levels of these metals. As illustrated in
Fig. 3, filter feeder fish, such as sardine, have lower Hg concentrations
(0.1 mg kg− 1) than largehead hairtail, Trichiurus lepturus
(0.67 mg kg− 1), who feeds on molluscans and other fish. Additionally,
the concentration of the same metal in F. magnificens, which is at the top
of the food chain, was considerably higher (8.39 mg kg− 1). It should be
noted that the assessed fish in the current study have economic
importance. Thereby, Hg accumulation has received considerable
attention, and mounting evidence suggests that organisms from the
higher trophic levels accumulate more Hg than the lower trophic levels
of the food web (Houserova et al., 2007). Carrasco et al. (2011a) and
Carrasco et al. (2011b) found this tendency in fish from the basin of the
lower Ebro (NE of Spain). In contrast, Pb and Cu exhibited different
profiles (see Fig. 3), probably as a consequence of the low Pb
bioavailability in sediments in the Cispata Bay, as noted by
Paternina-Uribe (2011).
Finally, the results observed in our study show a correlation
between the PAH concentrations in fish and seabirds from Cispata
Bay, indicating a common source of contamination, as confirmed by
established relationships. HMW-PAH were concentrated in sediments,
in contrast to that in the analysed fish and seabirds.
In conclusion, the results of the current study provide information
on the status of HM and PAH in the Cispata Bay. We determined the
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Marine Pollution Bulletin 120 (2017) 379–386
PAH concentration in blood from seabirds, fish, sediments and water
samples from the Cispata Bay. The assessed indices for the determina-
tion of the contamination source indicated a petrogenic origin with
biogenic influence for all sampling points. PAH concentrations in the
current study were lower than those reported in polluted areas;
however, chronic oil spills in the study area impose risk to the estuarine
ecosystem and the associated biota.
On the other hand, HM concentrations in the blood and feathers of
seabirds confirmed the presence of Hg and Pb and an increased level of
Cu and Zn, although these species also play metabolic roles in marine
organisms. There was no relation between the HM concentration and
hydrocarbon pollution; hence, these species enter the ecosystem from
anthropogenic inputs, such as runoff or transport through the lagoon
system that forms part of the Cispata Bay.
Appendix A. Supplementary data
Supplementary data to this article can be found online at http://dx.
doi.org/10.1016/j.marpolbul.2017.05.016.
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