Environmental Toxicology and Chemistry, Vol. 26, No. 8, pp.

15721581, 2007
2007 SETAC
Printed in the USA
0730-7268/07 $12.00 .00

EVALUATING MERCURY BIOMAGNIFICATION IN FISH FROM A TROPICAL MARINE

ENVIRONMENT USING STABLE ISOTOPES (13C AND 15N)

HASSAN A. AL-REASI,* FUAD A. ABABNEH, and DAVID R. LEAN

Department of Biology, Department of Chemistry, P.O. Box 450 Station A, University of Ottawa, Ottawa, Ontario K1N 6N5, Canada

( Received 18 July 2006; Accepted 14 February 2007)

AbstractConcentrations of total mercury (T-Hg) and methylmercury (MeHg) were measured in zooplankton and 13 fish species
from a coastal food web of the Gulf of Oman, an arm of the Arabian Sea between Oman and Iran. Stable isotope ratios (13C and
15N) also were determined to track mercury biomagnification. The average concentration of T-Hg in zooplankton was 21 8.0
ng g1 with MeHg accounting 10% of T-Hg. Total mercury levels in fish species ranged from 3.0 ng g1 (Sardinella longiceps) to
760 ng g1 (Rhizoprionodon acutus) with relatively lower fraction of MeHg (72%) than that found in other studies. The average
trophic difference (13C) between zooplankton and planktivorous fish (Selar crumenopthalmus, Rastrelliger kanagurta, and S.
longiceps) was higher (3.4) than expected, suggesting that zooplankton may not be the main diet or direct carbon source for
these fish species. However, further sampling would be required to compensate for temporal changes in zooplankton and the influence
of their lipid content. Trophic position inferred by 15N and and slopes of the regression equations (log10[T-Hg] 0.13[15N]
3.57 and log10[MeHg] 0.14[15N] 3.90) as estimates of biomagnification indicate that biomagnification of T-Hg and MeHg
was lower in this tropical ocean compared to what has been observed in arctic and temperate ecosystems and tropical African
lakes. The calculated daily intake of methylmercury in the diet of local people through fish consumption was well below the
established World Health Organization (WHO) tolerable daily intake threshold for most of the fish species except Euthynnus affinis,
Epinephelus epistictus, R. acutus, and Thunnus tonggol, illustrating safe consumption of the commonly consumed fish species.

KeywordsGulf of Oman Total mercury Methylmercury Trophic positions Fish

INTRODUCTION Mercury biomagnification and stable isotopes

Mercury (Hg) is a global pollutant due to emission and
long-range transport of the elemental mercury (Hg0) from both
natural and anthropogenic sources [1]. Due to the predomi-
nance of this form in the atmosphere with a long residence
time (1 year), it is capable of long-range transport with at-
mospheric deposition of Hg2as the source of contamination
to the aquatic ecosystems [2]. Consequently, Hg has been de-
tected in biota even from pristine ecosystems where no direct
mercury disposal has occurred [1]. Marine aquatic ecosystems,
covering approximately 70% of the earths surface, are exposed
to large-scale deposition of the Hg2, but conversion to meth-
ylmercury (MeHg) must take place prior to uptake and bio
magnification. Large predatory marine fish tend to contain
elevated MeHg concentrations of one to nine orders of mag-
nitude higher than that found in the water they live in (U.S.
Environmental Protection Agency [3]).
Mercury shows a tendency to increase from lower to higher
trophic levels, a phenomenon referred to as Hg biomagnifi-
cation. This is defined as a progressive accumulation of Hg
along the food chain. Methylmercury accumulation in the base
of the food chain was found to be the ultimate determinant of
mercury fish burden [4]. In addition, longevity and size pa-
rameters are the frequently reported factors believed to govern
Hg concentrations of fish tissues [57]. Feeding habits also
have a significant influence on Hg burden of fish. For example,
in similar-sized individuals, de Pinho et al. [7] observed that
the piscivorous shark species (i.e., feeding on fish) had higher
total mercury (T-Hg) concentrations than the shark species
feeding on benthic invertebrates.
* To whom correspondence may be addressed
(alreasi@squ.edu.om).
1572
Trophic structures and mercury biomagnification have been
investigated using traditional gut content analyses combined
with dietary observations of fish species. However, stable iso-
topes of carbon (13C) and nitrogen (15N) have emerged as
an alternative method of quantifying trophic structure. Unlike
the snapshot of stomach contents, isotopic signatures of tissues
provide an integration of the assimilated carbon over time and
can be used to track carbon flow between species since the
13C shows a trophic enrichment of only 0.5 to 1 between
diet and consumer for different ecosystems [8,9]. In spite of
the small magnitude, 13C values have been useful to connect
prey (i.e., diet) to predator (i.e., consumer). This enrichment
between prey and predator has been attributed to preferential
loss of 12CO2 during respiration, favored biochemical uptake
of 13C-compounds during digestion, and metabolic fraction-
ation during synthesis of different tissue types [10,11].
Unlike 13C, 15N undergoes substantial enrichment (av-
erage of 3.1) at each trophic level [12] and is highly cor-
related with Hg-biomagnification in several freshwater and
marine ecosystems. Several studies have been dedicated to
tropical freshwater ecosystems, particularly African lakes like
Lake Malawi [13] and Lake Victoria [14], East Africa, which
have been examined intensively. Studies have concluded that
mercury of biota shows biomangnification as predicted by their
15N-values. In the marine ecosystems, studies contended Hg-
biomagnification in long, well-characterized food webs in arc-
tic and temperate regions of the globe [15,16].
Few studies have been conducted for tropical marine eco-
systems; however, African tropical lakes have been investi-
gated extensively [13,14] and have contributed to our under-
standing of Hg behavior, fate, and transport of Hg in freshwater
Mercury biomagnification in the Gulf of Oman
Fig. 1. Map of the Gulf of Oman showing the study area.
systems. Here we examine the tropical aquatic ecosystem of
the Gulf of Oman, the northern part of the Arabian Sea situated
between Oman and Iran. This region is extremely arid with
very low precipitation levels. The Gulf supports a high di-
versity of phytoplankton [17], zooplankton, particularly co-
pepods [18], and many fish species (a total of 1,142 species
have been identified from the Gulf of Oman and Arabian Sea).
Stable isotope carbon (13C) and nitrogen (15N) were used in
conjunction with known feeding strategies to construct trophic
food web for zooplankton and several fish species in relation
to T-Hg and MeHg concentrations. Because the people of
Oman usually consume fish daily and fish consumption rep-
resents the main exposure route of methylmercury, we used
our fish mercury data to calculate consumption levels that do
not exceed the tolerable daily limit of consumption set by the
World Health Organization (WHO).
MATERIALS AND METHODS
Sample collections
Samples of zooplankton and different fish species were col-
lected between the end of May and June 2004 in the coastal
waters of ASeeb and Matrah, approximately 40 km apart (Fig.
1) near the capital of Muscat, Sultanate of Oman. A total of
27 zooplankton samples (18 for ASeeb and 9 for Matrah) were
collected using a 250-m mesh net that was towed horizontally
by the vessel. After each collection, the samples were poured
into 1-L plastic bottles with an excess amount of seawater and
Environ. Toxicol. Chem. 26, 2007 1573
stored in a cooler on ice. Within 1.5 h, the samples were
processed in the laboratory. The excess seawater was decanted,
and zooplankton were transferred to 15-ml plastic tubes with
a little amount of seawater and kept frozen at 20C. Micro-
scopic examination revealed that samples were composed
dominantly of copepods and a few larval shrimps.
Thirteen fish species (12 bony fish and 1 elasmobranch
species) were collected (Table 1) because they frequently are
consumed by the population and commonly encountered by
fishermen. Some demersal fish species were collected by tow-
ing at depth range of 20 to 40 m. Additional fish species were
purchased from the artisanal fishermen at the two cities. Fish
were stored in a cool box on ice and transported to laboratory
where they were identified, and measurements of total length
and weight were recorded. Then, based on the fish size, 10 to
15 g of boneless, skinless, left-side dorsal muscle were ob-
tained using scalpel and forceps and placed in 15-ml Falcon
(BD Biosciences, Franklin Lakes, NJ, USA) polyethylene
tubes known to be mercury free. Dissecting tools were washed
with 10% HNO3 and deionized water after each fish was pro-
cessed and a new scalpel was used for each fish species. The
samples were stored frozen at 20C. The samples were cov-
ered with dry ice in a properly sealed cooler and shipped to
University of Ottawa using air cargo (36 h of travel time). The
age of only three fish species (Carangoides malabaricus, Selar
crumenophthalmus, and Argyrops spinifer) were determined
using technique described by Secor et al. [19]. In brief, both
1574 Environ. Toxicol. Chem. 26, 2007 H.A. Al-Reasi et al.

Table 1. Range of size (length and weight) and age of the investigated fish species from the Gulf of Oman

Fish species Common names Symbol n Length (cm) Weight (g) Age (year)

Zooplankton 27
Sardinella longiceps Indian oil sardine O 16 15.417.0 3443 NDa
Selar crumenophthalmus Bigeye scad 13 15.526.7 34208 314
Carangoides malabaricus Malabar jack # 12 21.931.5 137418 311
Nemipterus randalli Randhals threadfin bream 12 21.829.8 70159 ND
Argyrops spinifer King solider bream 12 23.029.4 261560 314
Upeneus doriae Gilded goatfish 9 24.829.1 162264 ND
Rastrelliger kanagurta Indian mackerel 12 27.730.0 257340 ND
Scomberoides tol Needlescale queenfish 12 37.545.0 327566 ND
Epinephelus epistictus Dotted grouper y 12 33.548.8 5691,784 ND
Euthynnus affinis Kawakawa 9 46.063.2 1,2792,964 ND
Sphyraena sp. Barracuda 11 45.074.5 4641,537 ND
Thunnus tonggol Longtail tuna @ 10 69.078.4 3,6854,994 ND
Rhizoprionodon acutus Milk shark 7 66.585.0 1,1653,275 ND
a ND Not determined.

sagittal otoliths were removed from fish, cleaned in water, and
then air-dried. These sagittal otoliths were embedded in epoxy
resin and sectioned transversely. The sections were mounted
on glass slide and examined under light microscope. Incre-
ments were counted and each one consisting of opaque and
translucent zones represents a year. The restriction to three fish
was due to the difficulty in dissecting skulls and removing
sagittal otoliths of some fish, especially pelagic species, which
were fragile and easily broken, making some otoliths not read-
able.
Stable isotope analyses
Zooplankton samples were lyophilized by freezer dryer, and
fish tissues were oven-dried at temperature range of 60.0 to
61.5C for 24 h. The dried materials were homogenized into
a fine powder using a porcelain mortar and pestle. The pow-
dered samples then were stored in closed scintillation vials
that were kept in a desiccator. Zooplankton (8001,000 g)
and fish (700 g) samples were transferred to 3.5- 5.0-mm
tin capsules (Elemental Microanalysis Limited, Iso-mass Sci-
entific Incorporation, Calgary, AB, Canada). Isotopic com-
positions (13C/12C and 14N/15N ratios) were analyzed using an
elemental analyzer, EA1110 (Carlo Erba Instruments, Milan,
Italy) connected to an isotope ratio mass spectrometer (DeltaPlus
Advantage isotope ratio mass spectrometer, ThermoFinnigan,
Bremen, Germany). The heavy isotopic concentrations were
quantified relative to a standard reference material (Pee Dee
Belemnite for carbon and atmospheric N2 for nitrogen) and
expressed using the part per thousand () notation calculated
according to
mine the samples total mercury. After combustion at 850C,
mercury is converted catalytically to elemental mercury. Fol-
lowing dual gold amalgamation, the quantity of mercury is
measured by the cold vapor atomic absorption method at a
wavelength of 253.7 nm. The samples required no chemical
treatment prior to the analysis. Up to 32.2 mg of dried zoo-
plankton samples and between 10 to 100 mg wet fish samples
were placed on a layer of an additive (mixture of sodium
carbonate and calcium hydroxide; EMD Chemicals, Gibbs-
town, NJ, USA) in a ceramic boat as suggested by the supplier.
The sample then was covered with a layer of the same additive.
A layer of aluminum oxide ([Al2O3], EMD Chemicals) was
placed over the sodium carbonatecalcium hydroxide layer.
This aluminum oxide layer was covered by another layer of
the latter one. After that, the boat was transferred manually
into the ceramic thermal decomposition chamber. Reproduc-
ibility and accuracy of the method was assessed every 5 sam-
ples using a standard of 2.0 ppb and nondefatted lobster he-
patopancreas (National Research Council Canada, Ottawa,
ON, Canada). The found and certified values of nondefatted
lobster hepatopancreas were 0.116 0.007 (n 37) and 0.112
0.015 g g1 dry weight, respectively.
MeHg analyses
Determination of MeHg concentration was carried out by
capillary gas chromatography coupled with atomic fluores-
cence spectrometry [20]. Approximately 0.3 g of composite
freeze-dried zooplankton samples and between 0.05 and 0.1 g
of wet weight fish samples were placed in 20-ml scintillation
vials with Teflon polytetrafluoroethylene caps. Then, 2.0 ml

x
[
Rsample

Rreference ]
1 1,000
of deionizied water and 2.0 ml of 6 N potassium hydroxide
solution were added and the samples were shaken for 4 h at
300 rpm. After that, 2.0 ml of 6N hydrochloric acid were added
where x is C or N and R is the corresponding ratio 13C/12C
13 15
and the pH was checked to be 3.0 (high acidic medium).
or 15N/14N. Four millimeters of mixture (acidic [5% v/v H2SO4] potassium
Reproducibility of the method was checked using three bromide/1.0 copper sulfate) were added. To extract MeHg into
internal standards (caffeine, glycine, and methionine). Tripli- the organic phase, 5.0 ml of methylene chloride was added
cate samples of the internal standards were analyzed just after and the vials were shaken overnight at 300 rpm. The next day,
the blank and after every eight samples. The 2- standard the samples were centrifuged for 10 min at 2,500 rpm. A 2.0-
deviation for the internal standards was 0.20 for both 13C ml aliquot of the methylene chloride was transferred to 7-ml
and 15N. glass tubes and 1.0 ml of 0.01 M sodium thiosulfate was added
to each sample. The samples were shaken for 20 min, mixed
T-Hg analyses on a vortex mixer, and centrifuged for 5 min at 5,000 rpm. A
An automatic mercury analyzer, MERCURY SP-3D ana- volume of 0.4 ml of the aqueous top layer (sodium thiosulfate)
lyzer (Nippon Instruments, Osaka, Japan), was used to deter- was placed in polyethylene microcentrifuge vials and 0.3 ml
Mercury biomagnification in the Gulf of Oman Environ. Toxicol. Chem. 26, 2007 1575

Table 2. Carbon and nitrogen isotopic compositions (mean standard deviation), range of total mercury (T-Hg) and methyl mercury (MeHg)
concentrations (wet weight), and proportion of MeHg of zooplankton and fish species collected from the Gulf of Oman. *Composite samples

Fish species Symbol n 13C () 15N () T-Hg (ng g1) MeHg Mean % (range)

Zooplankton 27 19.87 1.74 11.16 1.30 1037

5* 0.11.9 10 (119)
Sardinella longiceps O 16 16.35 0.21 14.74 0.47 35 24 70 (4896)
Selar crumenophthalmus 13 16.79 0.63 14.27 0.73 699 295 70 (3597)
Carangoides malabaricus # 12 14.94 0.58 17.03 0.85 13108 693 73 (4792)
Nemipterus randalli 12 16.05 0.17 15.25 0.60 1546 1141 67 (5489)
Argyrops spinifer 12 15.77 0.51 16.00 0.21 20212 16169 79 (6188)
Upeneus doriae 9 14.38 0.69 15.88 0.66 1242 741 73 (4198)
Rastrelliger kanagurta 12 16.68 0.28 14.63 0.46 38 27 79 (5392)
Scomberoides tol 12 16.20 0.16 14.78 1.08 2859 1332 53 (3368)
Epinephelus epistictus y 12 16.49 0.78 17.05 0.46 59199 25192 82 (4397)
Euthynnus affinis 9 16.80 0.61 13.70 0.68 51309 26222 60 (37100)
Sphyraena sp. 11 15.60 0.57 17.72 0.48 17143 10118 77 (3696)
Thunnus tonggol @ 10 16.36 0.65 16.51 0.87 122184 94176 86 (7199)
Rhizoprionodon acutus 7 15.15 0.20 17.39 0.39 33760 24407 71 (3999)

of acidic potassium bromide/1.0 copper sulfate mixture and
0.5 ml of dichloromethane were added. Again, the vials were
shaken for 15 min, mixed, and centrifuged. Finally, the lower
phase (dichloromethane containing the extracted MeHg) was
extracted carefully and transferred through a small layer of
anhydrous sodium sulfate (packed in a pipette tip) to a 2-ml
amber glass vial with a 200-l glass insert. One standard and
a certified reference material (dogfish muscle certified refer-
ence material for trace metals, National Research Council Can-
ada) were run every five samples to evaluate reproducibility
and accuracy of analysis method. The average recovery of the
spiked samples (n 54) was 92 12% (70114%). The
experimental value found for dogfish muscle certified reference
material for trace metals was 4.15 0.57 mg kg1, which
represents 92% of the certified value (4.47 0.32 mg kg1).
Statistical analyses
Data were statistically analyzed using Statistical Package
for the Social Sciences for Windows (Ver 11.0.0, 2001, SPSS,
Chicago, IL, USA). The degree of significance for statistical
analysis was established at the 0.05 level. Nonparametric Ken-
dalls tau () coefficient was used to test correlations between
the values (length, weight, age, 13C, 15N, T-Hg, and MeHg).
Differences between species were analyzed by KruskalWallis
(H), a nonparametric equivalent to analysis of variance, fol-
lowed by a nonparametric post hoc procedure, Mann-Whitey
test (U). Nonparametric methods were used not only because
of non-normal distribution of data, but also because they are
most appropriate for small sample sizes. The assumptions re-
quired by linear regression were violated and, therefore,
T-Hg and MeHg values were log-transformed.
RESULTS AND DISCUSSION
Isotopic composition of zooplankton
The 13C-values of zooplankton collected from ASeeb ex-
hibited wide range of variability (24.56 to 16.28) com-
pared to samples obtained from coastal water of Matrah
(19.71 to 19.06); however, no significant difference was
determined between the two cities (U 67, p 0.05). The
overall mean 13C-value of zooplankton (19.89 1.74)
was similar to values reported for copepods (20.80) and
euphausiids (19.80 0.40) for northwestern Atlantic [10],
and euphausiids (20.10 0.30) in the Gulf of Farallones
[15]. Compared to 13C, 15N-values of zooplankton in this
study were consistent for both cities with mean and standard
deviation of 11.21 1.27 (Matrah) and 11.13 1.34
(ASeeb). Zooplankton samples principally were constituted of
copepods, the most dominant and diverse group of zooplankton
for the Arabian Sea and Gulf of Oman [18]. The observed
values of 13C and 15N of zooplankton from the Gulf of Oman
could be related to the lack of permanent rivers or streams
flowing into the gulf and that terrestrial runoff due to heavy
flash rains is restricted to a few days a year [21]. Therefore,
incorporation of terrestrial carbon and nitrogen, characterized
by light 13C and 15N concentrations, at the base of this coastal
marine food web seems unlikely. The wide variability exhib-
ited by 13C- and 15N-values suggests omnivory/carnivory
among copepods. Zooplankton samples collected from North-
east Water Polynya off eastern Greenland showed that herbiv-
orous copepods (Calanus hyperboreus) had an average 15N
of 7.9, and carnivorous copepods (Euchaeta glacialis) had
an average of 11.8 [22].
Isotopic carbon composition of fish species
Fish species showed a 13C range between 18.59 in the
grouper to 13.36 in the goatfish. The average 13C-values
for all species are presented in Table 2. A similar range
(18.60 to 13.4) was reported by Thimdee et al. [23] for
different fish species from the tropical marine ecosystem of
Khung Krabaen (Thailand). Yellowfin tuna (Thunnus alba-
cares) had a muscle 13C of 16.10 [24], almost the same
value (16.34) reported for its closely related longtail tuna
(Thunnus tonggol) from the Gulf of Oman. Also, the range
(18.59 to 15.94) of the grouper (Epinephelus epistictus)
was close enough to the documented range (17.90 to
15.90) for a close species, Epinephelus margintus, from
a western Mediterranean littoral ecosystem [25]. A significant
difference in 13C-values (H 102, degrees of freedom 12,
p 0.001) was observed among fish species. The most ele-
vated values were recorded in two predatory fish species, the
jack and shark, and the goatfish. On the other hand, the lowest
signatures were found, as predicted, in the planktivorous spe-
cies, sardines, scads and mackerels, and surprisingly in some
fish species identified as predators like kawakawa, longtail
tuna, and grouper. The heavy isotopic carbon signatures were
not related to length or weight of any of the investigated fish
species (H. Al-Reasi, unpublished data). The lack of relation-
ship between carbon signatures and size parameters (length
1576 Environ. Toxicol. Chem. 26, 2007
Table 3. Observed diet items of fish species collected from the Gulf of Oman. NA No available information on the diet items of this species
Fish species Symbol
Sardinella longiceps O Phytoplankton, zooplankton, and small crustaceans
Selar crumenophthalmus Zooplankton
Carangoides malabaricus # Crustaceans, small squids, and fish
Nemipterus randalli NA
Argyrops spinifer Benthic invertebrates
Upeneus doriae NA
Rastrelliger kanagurta Zooplankton
Scomberoides tol Fish
Epinephelus epistictus y Fish and crustaceans
Euthynnus affinis Small fish (clupeids and antherinids), squids and crustaceans and zooplankton
Sphyraena sp. Fish
Thunnus tonggol @ Fish, cephalopods, and crustaceans (stomatopod larvae and prawns)
Rhizoprionodon acutus Benthic and schooling fish (clupeids), cephalopods, crustaceans, and gastropods
and weight) for each fish species indicates that fish species
have food from primary producers with the same carbon sig-
natures and do not change as fish grow.
Isotopic nitrogen composition of fish species
The 15N-signatures of fish species ranged from 12.54
(kawakawa) to 18.48 in the jack and barracuda. The average
15N-values for all species are given in Table 2. A significant
difference was observed between isotopic nitrogen ratios of
fish species (H 118, degrees of freedom 12, p 0.001).
On average, the lowest 15N-values were found in tissues of
the planktivorous fish species. Some opportunistic predators
(jacks, sharks, and groupers) and the piscivore barracuda had
the most elevated 15N-values. King solider bream, tuna, and
goatfish had statistically similar 15N-signatures, as were scads,
Randhals threadfin bream, kawakawa, needle-scale queenfish,
sardines, and mackerels. It could be inferred that predator ka-
wakawa feed at a similar trophic level as planktivorous fish
species. Kawakawa is a highly opportunistic predator feeding
on variety of prey items (Table 3), and the reported lower
15N-values could be related to the feeding nature of this spe-
cies. The significant correlation between 15N-signatures and
length and weight of Kawakawa suggests a shift in feeding
habit from one prey item to another over time. A similar grad-
ual increase of trophic position was described for Epinephelus
margintus [25]. The lack of correlations for other fish species
probably could be related to limited individual sizes included
for each species.
Trophic isotopic fractionation
The trophic fractionation () of 13C between zooplankton
and planktivorous consumers averaged 3.4. On the other
hand, the 13C between sardines and their predator (shark)
was 1.2, an isotopic value close to the frequently reported
values of 0.50 to 1.0 [911]. The large 13C transfer between
zooplankton and planktivorous fish suggests that there should
be an additional trophic link(s). This implies that the zoo-
plankton might not be the main diet or direct carbon source
of these fish species. Alternatively, a benthic or littoral food
source for the fish is implicated. Great caution should be taken
with the previous conclusion of disconnection between zoo-
plankton and planktivorous fish species in term of energy trans-
fer as indicated by carbon isotope data. The trophic differences
of 15N between zooplankton and planktivorous fish species
and between the sardine and shark were 3.4 and 2.7, re-
spectively. These values are similar to those determined by
others [13,14] and consistent with that expected for prey
H.A. Al-Reasi et al.
Diet compositions Reference
[38]
[38]
[38]
[39]
[38]
[38]
[38]
[40]
[38]
[40]
[38]
predator relationships. Further sampling would be necessary
to clarify alternative feeding patterns, because direct feeding
on zooplankton might occur based on previous literature 13C
values in aquatic and marine food chains. Additional sampling
of invertebrates of this ecosystem would help resolve this issue
and provide more detailed information about this food web.
Moreover, limited temporal sampling of zooplankton may have
resulted in carbon isotope estimates that may not have been
representative of isotope signatures in the zooplankton com-
munity over a longer time period. In a western Mediterranean
lagoon, Vizzini and Mazzola [26] showed that carbon signa-
tures in zooplankton, particularly copepods, can vary greatly
through time, reflecting variations in phytoplankton signatures.
At the base of the food web, these variations do not manifest
themselves to the same extent in fish because of longer life-
spans and longer tissue turnover times [27]. Gut content anal-
yses would strengthen our understanding because it could pro-
vide evidence if the zooplankton were among items consumed
by the fish. Unfortunately, no gut content analysis was carried
out. Because lipids are depleted in 13C isotope, removal of
lipids could result in more negative 13C-values, hence there
is a larger difference between zooplankton and their consum-
ers. Indeed, copepods species have a higher content of lipids
than many other zooplankton species [28].
15N is useful in construction of the food web of a system;
however, utilizing 15N to compare webs of different systems
can be complicated due to difference of baseline 15N [29].
There would be a concern about analyses regarding trophic
positions would occur because samples were collected from
coastal water of two cities approximately 40 km apart and the
data set of 15N is not baseline corrected. However, this does
not imply difference in 15N at the base of food chains given
the similar 15N values of zooplankton (11.21 1.27 for
Matrah and 11.13 1.34 for ASeeb). In most marine eco-
systems, zooplankton usually occupy lower trophic positions
of the food chains. Analyzing trophic positions of zooplankton
and fish species could be achieved by interpretation of their
15N values, which can be useful in comparison of food webs
with common species [16] such as those collected from coastal
water of the two cities. Figure 2 illustrates that trophic position
of zooplankton is distinctly different from that of the fish spe-
cies. The trend in fish species distribution was consistent with
planktivores (the sardines, scads, and mackerels) occupying
relatively lower positions, invertivore (King solider bream) at
intermediate positions, and predators (the tuna, grouper, jack,
and shark) and the piscivore (barracuda) occupying higher
positions.
Mercury biomagnification in the Gulf of Oman
Fig. 2. Trophic positions determined by means of 13C and 15N sig-
natures () of zooplankton (n 27 samples) and 13 fish species (n
147 samples) from the Gulf of Oman. Bars represent standard
deviations (SD). Refer to Table 2 for SD of 13C and 15N and symbols
of fish species.
Mercury in zooplankton
Total mercury concentrations of zooplankton samples
ranged from 10 to 37 ng g1 wet weight. The mean concen-
trations (standard deviation) for samples collected were 20
8 and 22 8 ng g1 for Matrah and ASeeb, respectively.
The range reported in the present study was higher than that
(310 ng g1 wet wt) determined by Al-Majed and Preston [6]
for samples from Kuwait Bay, a northern embayment of the
Arabian Gulf. However, T-Hg range was well below that doc-
umented for polluted water bodies such as Bombay harbor
(103139 ng g1) [30]. The MeHg proportion of T-Hg spanned
from 1 to 19%. Methylmercury found in zooplankton samples
from Kuwait Bay accounted for 25% of T-Hg [6].
T-Hg and MeHg of fish species
Total mercury levels in fish species exhibited a broad range
between 3 ng g1 in the sardines and scads to 760 ng g1 in
the milk shark (Table 2). The average MeHg concentrations
of fish species ranged between 2 and 216 ng g1 in the sardines
and shark (Table 2). A significant difference was observed in
T-Hg concentrations of zooplankton and fish species (H 131,
degrees of freedom 13, p 0.001). Post hoc nonparametric
multiple comparisons demonstrated that zooplankton had
T-Hg levels significantly higher than those of the sardine and
mackerel (H. Al-Reasi, unpublished data). Despite the differ-
ence in size parameters (length and weight; Table 1), the scads
and mackerels had similar T-Hg levels. Total mercury con-
centrations of the shark demonstrated high variability but its
T-Hg concentrations were not statistically different from those
of other predatory species, the kawakawa (U 19, p 0.05),
tuna (U 15, p 0.051), and grouper (U 16, p 0.05).
The jack, threadfin bream, barracuda, and goatfish had similar
tissue T-Hg levels. A significant difference was detected in
MeHg concentrations between the investigated fish species (H
111, degrees of freedom 12, p 0.001). Follow-up non-
parametric comparisons revealed that the sardine and mackerel
had similar MeHg levels, as did king solider bream, kawakawa,
shark, barracuda, grouper, and goatfish. Methylmercury bur-
Environ. Toxicol. Chem. 26, 2007 1577
dens of the jack, scad, threadfin bream, and queenfish were
not statistically different (H. Al-Reasi, unpublished data).
Methylmercury is the dominant chemical species of mer-
cury accumulated in higher concentration in biota, especially
at higher levels of the food web. In the Gulf of Oman, zoo-
plankton showed higher T-Hg concentrations than the plank-
tivorous fish (sardine and mackerel). On the other hand, the
latter had higher proportions (range: 4896%) of MeHg than
zooplankton (mean 10%). This may suggest low contri-
bution of waterborne organic mercury to either zooplankton
or fish species. This would imply that direct uptake of MeHg
from water is unlikely or at least minimal compared to that
received via food. Hammerschmidt and Fitzgerald [31]
claimed that much of MeHg in higher trophic levels of coastal
marine ecosystems may be attributed to net MeHg sedimentary
production. Mercury concentrations in sediments along the
Gulf of Oman ranged from 0.1 to 0.9 ng g1 wet weight
[32], which are generally low compared to 46 and 100 ng g1
dry weight reported for Lake Malawi [13] and Lake Victoria
[14], respectively. Sediment contribution either to water col-
umn or fish burden would be expected to be limited. Appar-
ently, there have been no known sources of anthropogenic
mercury input into the Gulf of Oman unless the contribution
of the three major industries (oil refinery, water desalination
and electricity production plant, and the oil-tanker port) sit-
uated along the coast between the two cities.
In fish, T-Hg exits dominantly in methylated form or MeHg.
Fish species had considerably variable MeHg concentrations
with overall average of 72% of T-Hg (Table 2). The range of
%MeHg (33100) is similar to that reported by Al-Majed and
Preston [6] for seven fish species from a nearby aquatic tropical
body, the Kuwait Bay. In tropical marine ecosystems, wide
variability of %MeHg in fish tissues largely could be attributed
to the dietary exposure. Hall et al. [33] stated that mercury
accumulation from diet items is responsible for elevated Hg
burden. In complex food web, tropical fish species including
those in the present study survive on diverse prey items (Table
3). Variation in MeHg contents of their prey items would con-
tribute to high variability of MeHg burden of fish species [31].
The fish concentration of MeHg largely depends on selection
of prey items by individual fish, and ontogenic or shift in
feeding habit also would influence MeHg concentration [31].
Some fish species tend to change their prey items as they grow;
therefore, size and longevity are pronounced factors affecting
not only T-Hg concentrations but also variability in MeHg
accumulation. In addition, fish species of higher trophic levels
are more likely to be migratory and have larger foraging ranges
than low trophic ones [16]. Interspecific differences in move-
ment pattern could account for variability in mercury exposure.
For example, sardines (planktivore) showed a relatively lower
%MeHg range than kawakawa (migratory tuna species).
Mercury biomagnification
A weak significant linear relationship was determined be-
tween log10(T-Hg) and 15N-signatures (r2 0.09, p 0.0001;
Fig. 3A) for zooplankton and fish species from the Gulf of
Oman. However, on exclusion of zooplankton data the rela-
tionships improved slightly and were described by the regres-
sion equations for T-Hg and MeHg as: log10(T-Hg)
0.13(15N) 3.57 and log10(MeHg) 0.14(15N) 3.90 (Fig.
3B), respectively. The slope of the regression (0.07) of the
log-transformed T-Hg concentrations and 15N values, as bio-
magnification power, is substantially smaller than the 0.32 de-
1578 Environ. Toxicol. Chem. 26, 2007
Fig. 3. Relationship between trophic positions, determined by 15N,
and logarithm of total mercury (A) and logarithm of methylmercury
(B) concentration in zooplankton and fish species from the Gulf of
Oman. Refer to Table 2 for symbols of zooplankton and fish species.
termined by Jarman et al. [15] in the Gulf of Farallones and
0.20 found for the marine food web of Lancaster Sound, Nu-
navut, Canada [16]. It is also lower than the slope range (0.17
0.48) reported by Kidd et al. [34] for fish species from six
temperate lakes in northwestern Ontario, Canada. Total mer-
cury biomagnification also was observed in tropical lakes, as
estimated by slopes of 0.20 to 0.25 for Lake Malawi [13] and
0.16 to 0.17 for Lake Victoria [14]. After exclusion of zoo-
plankton data, the slopes (0.13 for T-Hg and 0.14 for MeHg)
are still smaller in magnitude in this tropical ocean compared
to those reported for temperate and arctic marine [15,16] and
freshwater ecosystems [13,14,34], indicating lower extent of
Hg-biomagnification at each trophic level.
In the Gulf of Oman, the weak relationship (r2 0.09 and
0.11) between mercury concentrations and 15N values con-
tradicts what has been found in temperate [15,34], arctic [16],
and tropical freshwater ecosystems [13,14]. The sample set
may raise concern about this observation, because it focused
on fish commonly encountered by fishermen and consumed by
population. However, this contradiction could not merely be
attributed to the sample set because it also had zooplankton
samples, and fish species represent different feeding habits
with reasonable sample size (n 716). Campbell et al. [35]
H.A. Al-Reasi et al.
found a significant relationship between log10(T-Hg) and 15N
for a sample set of only fish (n 19) and one crustacean
species from Thruston Bay, Lake Victoria. Lower biomagni-
fication in this tropical ocean would be attributed to the fact
that tropical marine ecosystems are characterized by complex
food webs and species diversity and abundance that would
imply different food sources (Table 3) with variable mercury
burden available for fish species. Variable concentrations in
zooplankton and other invertebrates transferred via feeding to
their consumers (fish) would result in a highly variable burden.
Fish having similar 15N values and highly variable T-Hg and
MeHg concentrations (Table 2) would lead to lack of biomag-
nification trend. This does not only highlight the influence of
species composition but also bioavailability of mercury at the
base of the food chain, which might be another possibility to
explain the weak relationship between trophic positions in-
dicated by 15N and mercury concentrations.
Mercury burden of fish generally is affected by several
variables including age, size, and trophic position. For age, no
significant correlation was detected with T-Hg for Malabar jack
( 0.119, p 0.643), bigeye scad ( 0.109, p 0.708),
or king solider bream ( 0.241, p 0.309). Similar to
T-Hg, their MeHg levels were not related to age. Neither
T-Hg nor MeHg concentrations were related to their age, al-
though it covered a range of 3 to 11 years for Malabar jack,
3 to 13 years for bigeye scad, and 3 to 14 for king solider
bream, probably due to small sample size (n 1213) and
limited sizes of individuals. In more than 80 individuals of
barred sand bass (Paralabrax nebulifer), Philip et al. [5] de-
scribed a moderate correlation (r2 0.34) between age and
T-Hg. The insignificant correlation between age and tissue
mercury concentration also could be explained by the fact that
the growth of tropical marine fish is rapid and characterized
by high production of tissue in a short period of time [14].
Even with frequent exposure, continuous tissue accumulation
would dilute mercury burden and prevent development of re-
lationship between age and mercury concentration. Significant
positive correlations between T-Hg and length/weight were
observed for the jack, scad, shark, and grouper (H. Al-Reasi,
unpublished data). The goatfish showed positive correlation
between T-Hg and length ( 0.500, p 0.05), but not with
weight ( 0.370, p 0.118). Similarly, MeHg demonstrated
significant correlation with length and weight of the jack, scad,
kawakawa, and grouper. Methylmercury levels of the shark
only correlated to weight ( 0.781, p 0.05). The positive
relationships between T-Hg and MeHg and length/weight for
these fish indicates that T-Hg levels increase as they grow in
size, a trend frequently observed for fish [57]. Limited size
(Table 1) of individuals for other species, particularly sardine
and mackerel, cloaked the relationship between mercury bur-
den and size parameters. In addition, a significant positive
correlation was described between 15N-values and T-Hg (
0.636, p 0.05) and MeHg ( 0.527, p 0.05) for the
goatfish. A similar correlation was observed for MeHg con-
centrations of the kawakawa ( 0.556, p 0.05). Tissue
15N-values of the goatfish and kawakawa are indicators of the
influence of trophic position on their tissue mercury burden.
Supporting this conclusion, for the goatfish there was a sta-
tistically stronger correlation between T-Hg and 15N than that
with length ( 0.500, p 0.05), implying that mercury
burden of this species is more likely to be controlled by trophic
position than size. Interestingly, T-Hg and MeHg concentra-
tions were statistically positively related to 13C-signatures of
Mercury biomagnification in the Gulf of Oman Environ. Toxicol. Chem. 26, 2007 1579

Fig. 4. The calculated daily intake of methylmercury from fish species collected from the Gulf of Oman based on fishmeal of 50 and 75 g for
30-kg child (A) and 100 and 150 g for 60-kg woman (B). The calculated daily intake is compared to tolerable daily intake set by the World
Health Organization.
1580 Environ. Toxicol. Chem. 26, 2007
king solider bream ( 0.576, p 0.05 and 0.545, p MeHg. Mercury levels of fish species varied considerably, with
0.05, respectively) and sardine ( 0.454, p 0.05 and the lowest T-Hg (3 ng g1) found in sardine (planktivore) and
0.403, p 0.05, respectively).
Tolerable daily intake
For general human population, fish consumption represents
the dominant pathway of methylmercury exposure [36]. How-
ever, exposure depends on the species of fish consumed as
well as the quantity of fish eaten [36]. In the present study,
T-Hg concentrations were well below the WHO guideline for
total mercury (500 ng g1 wet wt), with the exception of two
samples (668 and 760 ng g1) of the milk shark. It is meth-
ylmercury, the most toxic form of mercury and neurotoxin,
that affects the development of the nervous system. To estimate
methylmercury intake through consumption of these fish spe-
cies, the results were interpreted in terms of the WHO tolerable
daily intake of 230 ng/kg body weight. Using daily fish meals
of 50 and 75 g for child of 30 kg, 100 and 150 g for child-
bearing age woman of 60 kg, and mean methylmercury con-
centrations in fish, the calculated daily intake ranged from 4
to 540 ng/kg body weight. Results are presented in Figure 4.
For their consumption determined, the calculated daily intake
of methylmercury was below the established WHO tolerable
daily intake for all fish species except kawakawa, grouper,
shark, and longtail tuna, all of which are predatory fish species.
The results found in this work are reassuring; however, it is
important to note that the estimated intake does not take into
account exposure from other sources. Moreover, higher fish
consumption would be of concern in terms of the risk of det-
rimental health effects.
The dietary pattern of Omani people living in different
regions (coastal and the interior) does not vary greatly in term
of diet composition and number of meals per day. In Oman,
consumption of fish is a common daily habit. The health risks
associated with methylmercury exposure through consumption
of fish are recognized. However, in this study, the mercury
levels in the species commonly consumed were low and intake
calculations showed that individuals could safely consume fish
when the type of fish is properly selected. Thus, the risk is
low whereas the benefits are numerous and cannot be over-
looked. Fish are excellent sources of high-quality protein and
low in saturated fat [36]. After industrial sector, the fisheries
are considered the most important nonoil source of income for
Oman. Moreover, the fishing industry still uses traditional
methods of harvesting fish and other seafood. More than
26,000 artisanal fishermen are employed directly in the fish-
eries sector [37] with fish landings of 118,877 metric tons
(86% of total fish landings) in 2003. These figures highlight
the economic importance of the traditional fishing activities.
CONCLUSION
In conclusion, concentrations of T-Hg and MeHg were mea-
sured in zooplankton and fish species collected from the Gulf
of Oman. Stable isotopes of 13C and 15N were determined
to track carbon flow and define trophic position of the species.
An average trophic difference (13C) of 3.4 was determined
between zooplankton and planktivorous fish, suggesting that
zooplankton would not be the main diet or direct carbon source
for these fish species. Further sampling should be conducted
to determine if zooplankton carbon isotopes vary sufficiently
with time.
Total mercury concentrations of zooplankton were low
(range: 1037 ng g1), with an average fraction of 10% as
H.A. Al-Reasi et al.
the highest (760 ng g1) found in shark (a predator). Lower
and variable percentages of MeHg (overall average: 72%)
would be related to lack of anthropogenic input, lower
contribution of sedimentary production, and diverse food
sources. As an estimate of biomagnification, slopes of the
regression equations, log10(T-Hg) 0.13(15N) 3.57 and
log10(MeHg) 0.14(15N) 3.90, indicate that biomagnifi-
cation of T-Hg and MeHg was lower in this tropical ocean,
probably due to diverse diet items with different mercury con-
centrations that resulted in similar 15N for each fish species
but highly variable mercury burden. This led to a weak re-
lationship between trophic position and mercury concentra-
tions, contrary to what has been observed in other arctic and
temperate ecosystems and tropical African lakes.
For fishmeal consumption of 50 and 150 g/d, the calculated
daily intake of methylmercury was below the established WHO
tolerable daily intake for all fish species except for four pred-
atory fish. These, however, could be consumed every 2 d. For
the Gulf of Oman, methylmercury levels in the fish species
commonly consumed are low and intake calculations showed
that individuals could safely consume fish.
AcknowledgementWe thank the technicians (N. Al-Abri, S. Al-Ku-
saibi, and S. Al-Shuili) at Department of Fisheries and Marine Sci-
ences, Sultan Qaboos University, for their help during sample col-
lection, species identification, and fish aging. We acknowledge people
at the G.G. Hatch Isotope Laboratories, Department of Earth Sciences,
University of Ottawa, especially P. Middlestead, W. Abdi, and P. Wick-
ham for their efforts during stable isotope analyses.
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