Post on 08-May-2023
Trophic Distribution of Cd, Pb, and Zn in a Food Web fromAltata-Ensenada del Pabellon Subtropical Lagoon, SE Gulf ofCalifornia
J. Ruelas-Inzunza Æ F. Paez-Osuna
Received: 14 August 2007 / Accepted: 22 October 2007 / Published online: 20 November 2007
� Springer Science+Business Media, LLC 2007
Abstract The aim of the work was to obtain a compara-
tive view of the trophic distribution of Cd, Pb, and Zn in
different organisms of the food web (from primary pro-
ducers to top predators), considering representative species
in Altata-Ensenada del Pabellon subtropical lagoon (SE
Gulf of California). The study provides the first quantitative
information on the biotransference of Cd, Pb, and Zn in a
moderately contaminated lagoon ecosystem. After exami-
nation of 31 trophic interactions, 20 cases resulted in
transference factors (TF) [ 1.0 for Cd, 14 cases for Pb, and
18 cases for Zn. For Cd, most of the TF [ 1 were found
mainly among the low trophic levels (15 of 20 links); for Pb,
most of the TF [ 1 were found mainly among the high
trophic levels (11 of 14 links), and for Zn, most of the
TF [ 1 were found mainly among the low trophic levels (14
of 18 links). This can be interpreted as partial evidence of
biomagnification of Cd, Pb, and Zn for the species involved.
The question of whether trace elements increase their
levels as a function of the trophic level is still a matter of
debate (Barwick and Maher 2003). Bioaccumulation of one
metal M (or other substance) is the process that causes an
increased concentration of M in an aquatic organism
compared to that in water, due to uptake by all exposure
routes (dietary absorption, transport across respiratory
surfaces, and dermal absorption). Biomagnification is
defined as a special case of bioaccumulation in which the
concentration of M in the organism exceeds that in the
organism’s diet due to dietary absorption (Mackay and
Fraser 2000). It is important to indicate that the increments
in metal concentration between the predator and prey found
in field studies are interpreted in terms of bioaccumulation
rather than biomagnification (Gray 2002).
Typically, it has been stated that mercury is subjected to
the bioaccumulation and biomagnification (Castilhos and
Bidone 2000; Dietz et al. 2000). In the case of other met-
als, several authors have reported biomagnification of
selenium (Biddinger and Gloss 1984) and zinc (Timmer-
mans et al. 1989), but other researchers have found that
biomagnification is nonexisting in the case of Fe, Zn, Mn,
Cu, Pb, Cd, Co, Ni, U, and Th (Amiard et al. 1980; Szefer
1991). Studies concerning the occurrence of trace metals
along food chains are still scarce, especially in tropical and
subtropical coastal ecosystems, where trophic relationships
are complex as a consequence of the elevated number of
species.
There is limited information regarding trace metal
behavior within Mexican coastal lagoons, particularly with
respect to biomagnification and biotransference. We have
previously reported that Altata-Ensenada del Pabellon
lagoon (AEPL) is moderately contaminated with Cd, Cu,
Mn, Pb, and Zn (Ruelas-Inzunza and Paez-Osuna 2004a,
2004b, 2006). On the basis of the trace metal pollution
problem for the region and considering the available
information on trace metal sources in the region, Cd, Pb,
and Zn were selected in the present study. An additional
factor is that in the intensive agriculture practiced in the
surroundings of the AEPL, great quantities of agrochemi-
cals are used (Carvalho et al. 1996), including fertilizers
J. Ruelas-Inzunza
Technological Institute of Mazatlan/Environmental Section,
P.O. Box 757, Mazatlan 82000, Sinaloa, Mexico
F. Paez-Osuna (&)
Universidad Nacional Autonoma de Mexico, P.O. Box 811,
Mazatlan 82000, Sinaloa, Mexico
e-mail: paezos@servidor.unam.mx
123
Arch Environ Contam Toxicol (2008) 54:584–596
DOI 10.1007/s00244-007-9075-4
and fungicides containing metals. The utilization of phos-
phorus-containing products such as fertilizers and
detergents has also been related to enrichment of heavy
metals in water bodies (Forstner and Wittmann 1979). The
fertilizers from phosphorite have higher contents of ele-
ments of environmental concern, such as Ag, As, Cd, Pb,
Se, and Zn (Otero et al. 2005); in the case of analyzed
elements in the present study, their enrichment factors
(from average shale) are among the highest, from 60 for Cd
to 2 in Pb and Zn (Altschuler 1980).
Other features of the selected elements are related to
their properties in biological systems (Bowen 1966) (e.g.,
the affinity of cations for organisms and their implications).
Metal ions are separated into class A, class B, and border-
line. Class A ion metals show an almost absolute preference
for binding to ligands with oxygen as the donor atom,
whereas class B metal ions seek out nitrogen and sulfur
centers in biological systems and often become irreversibly
bound there (Nieboer and Richardson 1980). The three
studied metals, Pb, Cd, and Zn, are borderline metal ions,
which are able to form stable complexes with all categories
of ligands. However, Pb and Zn, being both borderline ions,
have a more class B and class A character, respectively. Cd
is categorized in the center of the borderline class. In bio-
logical systems, these features have important implications;
Zn will have a preference for biomolecules, including
ligands such as carboxylate, carbonyl, alcohol, phosphate,
and phosphodiester, whereas Pb has a preference for ligands
such as sulfydryl, disulfide, thioeter, and amino.
Obviously, if the biomagnification of trace metals is
occurring, elevated trace metal concentrations in higher
trophic groups of organisms could pose a threat to organ-
isms themselves or to human consumers. In this study,
specimens of different trophic levels (from primary pro-
ducers to top predators) from a subtropical coastal lagoon
(AEPL) in the southeast Gulf of California were collected
in order to assess the trophic transfer and the biomagnifi-
cation of Cd, Pb, and Zn; analyses and statistical treatment
of data were made according to the approach of Barwick
and Maher (2003), which include a careful selection and
categorization of the species from the structure of the food
web, the ordinary sampling and metal analysis, and the
statistical treatment of metal data. This last stage covers, in
addition to routine statistical tests, classification and ordi-
nation techniques.
Materials and Methods
Study Area
The AEPL system is located on the northwest coast of
Mexico between latitudes 24� 200 and 24� 400 N and
longitudes 107� 300 and 108� 000 W (Fig. 1). It is only 2 m
deep on the average and consists of three embayments: (1)
Ensenada del Pabellon (232 km2), (2) Altata (75 km2), and
inner lagoons (Caimanero, 3 km2; Bataoto, 2 km2; and
Chiricahueto, 23 km2). The two main regions are con-
nected via a narrow channel where the Culiacan River
flows into. Agriculture effluents from 135,000 ha drain
indirectly via groundwater or directly via small channels
(esteros) into the principal lagoon system. Another source
of pollution is the urban sewage from the towns and cities
(925,000 habitants) surrounding the lagoon system.
Selection of Species
The structure of the lagoonal food web was derived from a
review of previous studies that have examined the gut
contents, feeding strategies, and habitat preferences of
organisms residing in the AEPL: birds (Calderon-Rodrı-
guez 2005), fish (Edwards 1978; Moriarty 1976; Ruiz-
Nieto 2005), and crustaceans (Dall et al. 1990; Edwards
1978). Considering the feeding habits, species were divided
into several groups: primary producers, detritivores, filter-
feeders, omnivores, and secondary and tertiary carnivores
(Table 1).
Most species were classified with sufficient confidence
into specific trophic groups. However, an issue in devel-
oping the food web was the difficulty in classifying various
species. This difficulty is related to changes in diet within
species through different stages of their life cycles.
Therefore, considering the stage of organisms during col-
lection (i.e., mainly adults), the classification was made
taking into account the predominant feeding habit. For
example, in adult shrimps Litopenaeus vannamei and Li-
topenaeus stylirostris, the diet is clearly omnivorous (Dall
et al. 1990; Edwards 1978). The detritivore Mugil cephalus
is also known to undergo a dietary shift upon reaching
maturity, from carnivorous to detritivorous (Moriarty
1976).
Sampling
Biota of different trophic levels was collected in three close
sites of the AEPL in the SE Gulf of California (Table 1,
Fig. 1). A total of 58 samples of aquatic organisms were
collected between December 1999 and February 2000. The
sampling included about 292 specimens of macroorgan-
isms and an undetermined number of specimens of
phytoplankton and macroalgae representing a total of 15
species (Table 1). Sampling strategy was designed for
evaluating elemental transference rates between some
important trophic links in the AEPL complex. Composite
Arch Environ Contam Toxicol (2008) 54:584–596 585
123
samples were taken far away from any immediate local
pollution sources; therefore, results could represent the
average of metal concentrations in biota. Individuals of
similar size within each species were selected to minimize
variations in metal concentration due to body size of the
organisms. Plankton was collected by using a plankton net
Fig. 1 Location of sites where
primary producers and
consumers of diverse levels
were collected in the AEPL.
Mangroves and areas covered
by shrimp farms are indicated
by black and dark-gray filled in
the surroundings of the lagoon
Table 1 Collected specimens of diverse trophic levels in the AEPL (SE Gulf of California)
Group Species Feeding
habit
Tissue Size range
(mm)
Individual
weight (g)
No. of pooled
organisms
No. of
pools
Sampling
location
Primary producers (sources)
Phytoplankton Coscinodiscus centralis Autotrophic Whole \118 lm – – 2 A
Macroalgae Gracilaria sp. Autotrophic Fronds – – – 2 B
Polisyphonia sp. Autotrophic Fronds – – – 2 B
Mangroves Rhizophora mangle Autotrophic Leaves 76–106 0.5–1.2 40 3 B
Avicennia germinans Autotrophic Leaves 76–117 0.9–1.6 40 4 B
Laguncularia racemosa Autotrophic Leaves 45–68 0.36–0.49 40 4 B
Primary consumers
Oysters Crassostrea corteziensis Filter-feeder Soft tissue 36–55 7.2–21.3 25 3 B
Barnacles Balanus eburneus Filter-feeder Soft tissue 11–23 1.4–7.3 60 3 B
Shrimps Litopenaeus stylirostris Omnivorous Muscle 155–193 28.3–48.9 40 3 B
Litopenaeus vannamei Omnivorous Muscle 141–164 17.0–27.7 40 2 B
Fish Mugil cephalus Detritivores Muscle 298–420 256–580 1 6 B
Secondary consumers
Fish Lutjanus colorado Carnivorous Muscle 220–440 159–1082 1 6 B
Cynoscion xanthulus Carnivorous Muscle 240–430 188–572 1 8 B
Tertiary consumers
Birds Pelecanus occidentalis Carnivorous Muscle 850–910 3500–3900 1 2 C
Phalacrocorax brasilianus Carnivorous Muscle 470–550 889–1057 1 6 C
Note: See Figure 1 for sampling locations A, B, and C
586 Arch Environ Contam Toxicol (2008) 54:584–596
123
(118-lm mesh size); towing of plankton net was carried
out slowly (2 knots) for *10 min. Five transects of 200 m
were conducted to obtain sufficient material for analysis.
Plankton samples were then placed in acid-washed plastic
bottles (Moody and Lindstrom 1977). Hundreds of com-
plete fronds of macroalgae were collected by hand during
low tides. Mangrove leaves (40 pieces) were collected by
hand. Macroalgae and mangrove samples were rinsed with
lagoon water to remove particulate material and placed in
acid-washed plastic bags. Oysters (75 individuals) and
barnacles (180 individuals) were separated and collected
from mangrove roots by using a stainless-steel knife.
Bivalve mollusks (Crassostrea corteziensis and Mytella
strigata) were placed in an aquarium with seawater supply
with aeration for a 24-h depuration period; in this way, the
food contents are expelled, avoiding the presence of metals
in the midgut (NAS 1980). In concordance with previous
studies, barnacles were not depurated (Phillips and Rain-
bow 1988; Rainbow et al. 1993).
Shrimps (200 individuals) and fish (1–8 individuals per
species) were collected using local commercial gill nets.
Birds (2–6 individuals per species) were shot using lead-
free ammunitions; a hunting permit from the official
authority in environmental matters was obtained (permit
SEMARNAT DOO.O2-3324) in order to collect the avi-
fauna. Birds were placed in individual plastic bags and in
similar manner all samples were placed on ice and trans-
ported to the laboratory.
Sample Preparation
Samples were stored at -18�C prior to analysis. With the
exception of birds, all samples were washed in situ with
seawater-brackish water at the time of collection. In the
laboratory, samples were washed with deionized water
(purified by reverse osmosis followed by ion-exchange
Milli-Q) to remove any particulate matter that might be
adhered. Organisms were then thawed at room temperature,
weighed, and sized. For fish, shrimp, bivalves, and barna-
cles, total length and individual weight were registered.
The common approach in biomagnification studies
includes the use of whole-body tissues in invertebrates and
phytoplankton (Gray 2002); in larger organisms, muscle is
commonly used. Here, the whole body was used for
chemical analysis whenever possible; that is, for phyto-
plankton, and macroalgae species, and in the case of
oysters and barnacles, the total soft tissue was used. In fish,
crustacean, and birds, muscle tissues were used for analy-
sis, as this is considered to represent the stable pool of trace
metals for these organisms (Barwick and Maher 2003).
Glassware and plastic materials used for handling and
transportation of samples were thoroughly acid-washed to
prevent contamination of samples (Moody and Lindstrom
1977). After taxonomic identification and determination of
length and weight of specimens, dissection with a stainless-
steel knife was performed in order to obtain the tissues of
interest. Samples were freeze-dried for 72 h at -49�C and
133 9 10-3 mbars in a Labconco freeze-drying system,
then powdered in an automatic agate mortar (Retsch) for
10 min. Powdered samples (0.25–0.5 g) were digested with
quartz-distilled concentrated nitric acid (5–10 mL) in a
microwave equipment (CEM, MDS 2000) under the con-
ditions given by MESL (1997).
Metal Analysis
Analyses were made by flame atomic absorption spectro-
photometry for Zn (working range of standards: 0–1.5 mg/
L); in the case of Cd and Pb (ranges of standards: 0–0.7 and
0–30 lg/L, respectively), graphite furnace atomic absorp-
tion spectrophotometry was used. Samples replicates
(n = 6) for each group of species and the different refer-
ence materials were run; the precision (expressed as
coefficient of variation) fluctuated from 2% to 5% for Cd,
from 6% to 11% for Pb, and from 3% to 8% for Zn.
Detection limits (three times the standard deviation) of the
analysed metals were estimated at 0.0002 mg/kg for Cd,
0.005 mg/kg for Pb, and 0.1 mg/kg for Zn.
Trace metals were quantified in a Varian SpectrAA 220
spectrophotometer equipped with deuterium background
correction. Levels of the different elements are expressed
as micrograms per gram on a dry weight basis. In order to
assess the accuracy of the employed method, reference
materials Fish Flesh MA-B-3/TM produced by IAEA-
MEL, Monaco (IAEA 1987), Mussel Tissue SRM 2977
(NIST 2000), and IAEA-331 Spinach (Zeisler et al. 1995)
were analyzed.
Concentrations of the analyzed elements were within
certified values of reference materials: The recovery in fish
was 86% for Cd, 96% for Zn, and 112% for Pb; in mussel,
it was 89% for Cd, 90% for Zn, and 110% for Pb; in
spinach, it was 94% for Cd, 101% for Zn, and 108% for Pb.
Details of the analytical procedure and the original con-
centration data for the examined metals have been
previously reported for penaeid shrimps (Ruelas-Inzunza
and Paez-Osuna 2004a), birds (Ruelas-Inzunza and Paez-
Osuna 2004b), and primary producers (Ruelas-Inzunza and
Paez-Osuna 2006).
Data Analyses
In order to have an idea of the degree of metal accumu-
lation in the analyzed species with respect to their
Arch Environ Contam Toxicol (2008) 54:584–596 587
123
surrounding environment, the concentration factor was
calculated according to the following formula (Szefer
1998): CF = C1/C2 , where C1 represents the average
concentration of the metal of interest in biota and C2 is the
average concentration of the element in the surrounding
surficial sediment. Metal concentrations for surficial sedi-
ments (collected in 1991) were taken from Green-Ruiz and
Paez-Osuna (2001).
Average concentrations of metals in the analyzed spe-
cies were used to calculate biomagnification or
transference factor (TF) according to Mackay and Fraser
(2000): TF = Cc/Cp, where Cc represents the concentration
of the metal (expressed on a dry weight basis) of interest in
the consumer (predator) and Cp is the concentration of the
metal in the food (potential prey). If the transfer factor
BMF [ 1, then the metal is biomagnified (Gray 2002).
Datasets were analyzed for normality using the Kol-
mogorov–Smirnov test and proved to be non-normal;
nonparametric Kruskal–Wallis tests were used to test the
significance of differences in mean metal concentrations
among trophic groups (Zar 1984). GraphPadPrism 4
package (San Diego, USA) was used to perform non-
parametric analyses. Classification and ordination
techniques were employed to examine groupings of spe-
cies based on their relative trace metal concentrations.
Classification involved the use of cluster analysis. The
results were then plotted on a multidimensional scaling
(MDS) ordination to examine patterns (Pielou 1975). The
differences between the metal concentrations and the
grouping were considered significant at levels of
p \ 0.05.
Results and Discussion
Table 2 and Figure 2 show trace metal concentrations in
the analyzed samples. In general, species of similar trophic
level and/or taxonomy can be grouped together given their
comparable metal content. Concentrations in the analyzed
organisms varied from 8.7 to 1420 mg/kg for Zn, from 0.5
to 4.9 mg/kg for Pb, and from 0.1 to 7.2 mg/kg for Cd.
Primary producers, such as mangroves, were characterized
by low Cd and Zn content. Macroalgae and phytoplankton
species also had low Cd concentrations but moderate Zn
levels. The filter-feeders oysters and barnacles had the
highest concentrations of Cd and Zn. Tertiary consumer
birds had from moderate to high Pb concentrations in
comparison to other consumers. The highest concentration
of Pb was found in Gracilaria sp., whereas the highest
concentration of Cd and Zn were found in the mollusc
Crassostrea corteziensis.
The fact that two species of primary consumers con-
centrated high values of Cd is not abnormal; through
laboratory experiments it has been shown that bivalves are
able to accumulate an elevated percentage of Cd due to
their ability to take the metal from the water column and
ingested particles (Wang et al. 1996). In connection with
crustaceans, a similar situation has been documented and
they appear to be unable to regulate Cd concentrations in
their bodies (Rainbow 1985). In the shrimp Crangon
crangon, Dethlefsen (1978) and Amiard et al. (1985) found
that Cd is accumulated in proportion to ambient
bioavailability.
Concentrations of lead in Coscinodiscus centralis from
this study were comparable to those reported in mesozoo-
plankton from the southern Baltic (Szefer et al. 1985) but
lower than values registered by George and Kureishy
(1979) in mixed plankton from the Bay of Bengal (up to
208 mg/kg). Concerning shrimps, results obtained here for
Pb were comparable to values reported in Litopenaeus
californiensis (0.4–0.45 mg/kg) from La Paz lagoon in the
SW Gulf of California (Mendez et al., 1997) but lower than
results (22.9 mg/kg) given in Penaeus monodon from
Sunderban, India (Guhathakurta and Kaviraj 2000). In the
case of Phalacrocorax brasilianus, the Pb mean reported in
this study (1.7 mg/kg) is higher than concentrations
(0.23 mg/kg) reported by Calderon-Rodrıguez (2005) in
the same species near the sampled site at AEPL (year
2002), which indicated that bioavailable Pb in this species
has a tendency to decrease in the region.
Zinc concentrations in mangrove oysters Crassostrea
corteziensis studied here were lower than Zn values
(1660 mg/kg) reported in the same species previously
collected from the same lagoon (Paez-Osuna et al. 1993a).
In relation to barnacles, several studies (e.g., Rainbow
1993; Rainbow and Phillips 1993) have documented their
potential as biomonitors of Zn; in a study with Balanus
eburneus in Mazatlan Harbor (a site with fish and shrimp
processing industry, canning of fish products, power plant
cooling systems, sandblasting of boats, and domestic
effluents from the city of Mazatlan), Ruelas-Inzunza and
Paez-Osuna (1998) reported that Zn values ranged from
5589 to 30,030 mg/kg and concluded that the study area is
polluted by this metal. In the present study, concentrations
of Zn in this species of barnacle ranged from 1182 to
1240 mg/kg.
The metal levels in all samples examined here might be
considered from moderate to high, as it would be expected
in an impacted area (Paez-Osuna et al. 2002). As it was
mentioned earlier, AEPL receives the discharge of
untreated sewage from numerous towns and Culiacan city;
additionally, agriculture and aquaculture effluents dis-
charge in this water body. Early studies (Paez-Osuna et al.
1993a, 1993b) have showed that oysters and clams had
elevated Cd, Cu, and Zn contents; such concentrations
were attributed to the agriculture activities where
588 Arch Environ Contam Toxicol (2008) 54:584–596
123
fungicides containing metals are applied. Green-Ruiz and
Paez-Osuna (2001), considering different criteria, exam-
ined the metal contents in surface sediments from the
lagoon system and found that about 90% of the polluted
sites (at least for Zn) occurred near agricultural discharge
drains. Similarly, the highest bioavailable (extracted with a
buffer solution at pH 5, prepared using a mixture of 1 M
water solution of CH3COONa and CH3COOH 25%) con-
centrations of metals were associated with agricultural
discharges and Culiacan River inputs. From these com-
parisons in the referred articles it has been mentioned that
the AEPL is moderated contaminated by Cd, Zn, and other
metals. Moderately polluted is certainly a relative concept;
in sediments, the enrichment factor and other indexes are
used. When such criteria combining metal concentrations
of the surface sediments with other metal background
levels (earth’s crust or pristine values) are considered, the
diagnostic is that sediments show low, intermediate,
moderate, or highly contaminated levels.
An alternative source of metals into the Gulf of Cali-
fornia region is related to upwelling waters, which are
enriched with nutrients and Cd and this might influence
metal availability in the study area. Delgadillo-Hinojosa
et al. (2001) concluded that the dissolved Cd distribution in
the Gulf is being controlled by a combination of biological
cycling, thermohaline circulation, and the mixing processes
at the midriff region.
The different feeding habits and living modes of shell-
fish, shrimp, fish, birds, barnacles, macroalgae, and
mangroves as well as the different aquatic geochemistry of
the trace metals affect the intake, assimilation, and sub-
sequent bioaccumulation of trace metals in these
organisms. Although the trace metal concentrations in
different species of aquatic organisms in the same trophic
group fluctuate widely, organisms in different groups also
showed significant differences in metal accumulation pat-
terns; in the case of Cd and Zn, significant differences were
found (Table 2, Fig. 2), which indicate that organisms in
different groups had different accumulation mechanisms
for trace metals.
Oysters and barnacles are filter-feeders and mainly use
fine suspended particulate matter as their food source. In
addition, these organisms are immobile or sessile and live
associated to the mangrove roots in the intertidal zone.
Based on the metal concentrations in the soft tissue of the
mangrove oyster Crassostrea corteziensis and the corre-
spondent concentrations in the dissolved and suspended
fractions of the lagoon waters, Paez-Osuna and Marmolejo-
Rivas (1990) found a direct relationship in which this
oyster reflects the metal levels in the suspended particulate
matter.
Among the different aquatic organisms, fish and birds
are probably the most mobile and capable of traveling a
long distance. However, fish collected in this study mainly
Table 2 Summary of trace metal concentrations (average ± standard deviation, mg/kg dry weight) in the different subgroups of collected
organisms in the AEPL (SE Gulf of California)
Group Species Species code Cd Pb Zn
Primary producers (sources) 0.24 ± 0.20a,b 2.3 ± 1.4 35 ± 35
Phytoplankton C. centralis CCE 0.27 ± 0.06 2.3 ± 0.3 117 ± 3
Macroalgae Gracilaria sp. GS 0.23 ± 0.01 4.9 ± 0.4 36.0 ± 2.2
Polisyphonia sp. PS 0.87 ± 0.30 3.1 ± 0.7 34.0 ± 3.0
Mangroves R. mangle RM 0.17 ± 0.04 2.1 ± 1.2 8.7 ± 1.3
A. germinans AG 0.10 ± 0.01 2.2 ± 1.0 21.0 ± 0.3
L. racemosa LR 0.25 ± 0.07 0.9 ± 0.3 15.0 ± 0.6
Primary consumers 2.1 ± 3.0a 1.6 ± 1.3 494 ± 645
Oysters C. corteziensis CCO 7.2 ± 2.8 3.4 ± 2.0 1420 ± 109
Barnacles B. eburneus BE 1.1 ± 0.1 2.1 ± 0.7 1210 ± 28
Shrimps L. stylirostris LS 0.5 ± 0.2 0.9 ± 0.3 61 ± 2
L. vannamei LV 3.1 ± 2.1 0.5 ± 0.1 53 ± 0.5
Fish M. cephalus MC 0.3 ± 0.3 1.0 ± 0.3 18.4 ± 0.9
Secondary consumers 0.6 ± 0.4 2.1 ± 1.2 18.1 ± 6.7
Fish L. colorado LC 0.2 ± 0.1 1.3 ± 0.8 21.0 ± 2.0
C. xanthulus CX 0.9 ± 0.1 2.6 ± 1.9 21.0 ± 3 .2
Tertiary consumers 0.9 ± 0.3b 2.9 ± 1.8 29.1 ± 8.3
Birds P. occidentalis POC 0.7 ± 0.1 4.2 ± 1.5 23.3 ± 5.0
P. brasilianus POL 1.2 ± 0.8 1.7 ± 0.9 35 ± 1 8
Note: Same letters indicate that means differ significantly (p \ 0.05) among trophic groups for a given metal
Arch Environ Contam Toxicol (2008) 54:584–596 589
123
live near the lagoon and with short traveling distance
(Lutjanus colorado and Cynoscion xanthulus). Further-
more, fish are also on a high trophic level in the food chain
compared to other types of organisms; hence, their diet is
probably the most diverse of the species studied here. For
example, L. colorado has a heterogeneous diet that consists
predominantly of fish (66.6%), crabs (23.2%), and shrimps
(10.6%) (Ruiz-Nieto 2005). In the case of the birds, the
studied species are presumably permanent residents of the
region (nonmigratory); they show a relatively elevated
mobility with a moderate traveling distance (Hamer et al.
2002). In the case of the birds Pelecanus occidentalis and
Phalacrocorax brasilianus, they are known to consume
elevated amounts of fish and shrimp (Mejıa-Sarmiento
2001).
Figure 3 shows transference factors (TFs) of Cd among
the different trophic links examined. From 31 calculated
transference rates, 20 cases were TF [ 1.0 (64.5%); the
highest transference factors were found in the links of
mangrove oyster Crassostrea corteziensis and the macro-
algae Gracilaria sp. (TF = 31.3) and C. corteziensis and
the phytoplankton species Coscinodiscus centralis (TF =
26.7). Litopenaeus vannamei was the second species that
accumulated more Cd, in which the TF = 31.0 with respect
to the link with mangrove Avicennia germinans. It might be
interpreted as evidence of Cd biomagnification in oysters
and shrimp. There were some evident trends in the mag-
nitude of biotransference factors between low and high
trophic groups. There were several food links that had
positive biotransference (TF [ 1) throughout its length,
indicating biomagnification: (1) from sediments or man-
groves (Avicennia germinans; Laguncularia racemosa;
Rhizophora mangle) to Litopenaeus stylirostris, to Cynos-
cion xanthulus, to Phalacrocorax brasilianus; (2) from
phytoplankton (C. centralis), and/or Polisyphonia sp., and/
or Gracilaria sp., and/or sediments to C. corteziensis or to
Balanus eburneus. Bargagli (1998) studied metal concen-
trations in a food web in the Mediterranean Sea and found
that at high trophic levels, Cd concentrations are lower than
at the bottom of the food chain, concluding that there is no
evidence of biomagnification of Cd in this marine food
chain. Similarly, Barwick and Maher (2003) found no
evidence of magnification of Cd in a temperate estuarine
ecosystem from NSW Australia; only in 5 of the 35 trophic
interactions examined did they observe increases in Cd
concentrations. Within the Greenland part of the Arctic,
Dietz et al. (2000) found a general pattern of Cd biomag-
nification, but the authors concluded that metal transfer in
successive trophic levels is influenced by the comparisons
being made among the different species. On the other hand,
in a study of TF in a southern Baltic ecosystem, it was
found that values for Cd were usually less than 1 (Szefer
1991).
Increases in Pb concentration among species occurred in
14 of the 31 trophic interactions examined (45.2%) (Fig. 4).
The highest transference rates were observed in the link
between the preys white shrimp (TF = 8.4) and mullet
(TF = 4.2) and the pelican Pelecanus occidentalis. Eleven
of the TF [ 1 (78.6%) were associated to the upper trophic
level, whereas in the lower levels, only three cases were
found. It shows that Pb is an element with small potential for
biomagnification or bioaccumulation from surrounding
waters at low trophic levels. There were only a few evident
trends in the magnitude of biotransference factors between
lower and higher trophic groups, indicating biomagnifica-
tion: (1) from mangroves (Laguncularia racemosa) to
Litopenaeus stylirostris, to Cynoscion xanthulus, to Phala-
crocorax brasilianus, to Lutjanus colorado; (2) from
Fig. 2 Trace metal concentrations in trophic groups of the AEPL
ecosystem. Mean ± SD. The same letter indicates that means differ
significantly (p \ 0.05) among trophic groups for a given metal
590 Arch Environ Contam Toxicol (2008) 54:584–596
123
phytoplankton (Coscinodiscus centralis) and/or Polisypho-
nia sp. to Crassostrea corteziensis.
From the number of potential trophic interactions with
values greater than 1 and considering that Pb usually
accumulates more markedly in sediments than in biota, it
can be said that this element is comparatively less likely to
be biomagnified. Dietz et al. (2000) have mentioned that
Pb does not accumulate toward higher trophic levels in the
terrestrial or the marine ecosystem; a similar pattern of
metal accumulation was found in diverse organisms from a
southern Baltic ecosystem (Szefer 1991)—the author con-
cluded that Pb is not biomagnified along the successive
trophic levels of the food chain.
Barwick and Maher (2003) found positive biotransfer-
ence of Pb in 9 of the 35 trophic interactions evaluated in a
temperate estuarine ecosystem from NSW Australia.
Considering that there were no evident trends in the mag-
nitude of biotransference factors between low and high
trophic groups and that only one food link had positive
biotransference throughout its length, they concluded that
there was no evidence of Pb biomagnification.
Concerning Zn, positive biotransference (TF [ 1) from
food sources to consumers occurred in 18 of the 31 trophic
interactions examined (58.1%) (Fig. 5). Contrary to lead,
most of the TF [ 1 were associated with the low trophic
levels (77.8%). All increases in mean Zn concentration
[i.e., elevated biotransference factors (TF = 41.8 and
39.4)] were those where the filter-feeders mangrove oyster
Crassostrea corteziensis (TF ranged from 12.1 to 41.8) and
barnacles Balanus eburneus (TF ranged from 33.6 to 35.5)
were involved. There were no systematic trends in the
magnitude of biotransference factors between low and high
trophic groups; perhaps Zn (being an essential metal) is
often regulated in organisms of higher trophic levels and
this might be interpreted as an insufficient evidence of Zn
biomagnification. This conclusion is consistent with the
Fig. 3 Biotransference and Cd
concentrations in AEPL
ecosystem components.
Concentrations within symbols
are mean concentrations (mg/
kg) and numbers on lines are
transference factors. For
sediments, numbers within
parentheses include bioavailable
metal concentration
Arch Environ Contam Toxicol (2008) 54:584–596 591
123
findings of Barwick and Maher (2003) in a temperate
seagrass ecosystem from the Lake Macquarie estuary in
Australia and with data reported by Szefer (1998) in biota
from a southern Baltic ecosystem.
Considering the characteristics of the aquatic birds
examined here and that the transference of trace metals via
abiotic routes is improbable, a biomagnification in the
upper trophic level birds might be visualized. In the other
organisms, it was difficult to discriminate the process of
biomagnification from bioaccumulation in the field because
the different organisms are in direct contact with the waters
and sediments from where metals might be accumulated.
Rodrıgues-dos Santos et al. (2006) found a small
increase of Zn content with increasing trophic level that
could be evidence of biomagnification in Admiralty Bay
organisms (Antarctica); in 26 of 27 transference rates,
values were greater than 1 (positive biotransference).
Similarly, positive biotransference from food sources to
consumers occurred in 8 of the 35 trophic interactions
examined by Barwick and Maher (2003) in a temperate
seagrass ecosystem from NSW Australia. However, these
studies indicate that such positive biotransference is related
very probably to bioaccumulation rather than to
biomagnification.
In subtropical ecosystems, biomagnification studies are
complicated because organisms have several food sources
with different concentrations, such is the situation in AEPL
organisms, which is notorious in the omnivorous Litope-
naeus vannamei and Litopenaeus stylirostris and the two
filter-feeders examined. Fish Lutjanus colorado and Cy-
noscion xanthulus are also characterized by consuming
several types of organisms (i.e., fish, crabs, and shrimp).
Additionally, migration and mobility of the organisms
complicate interpretation; in the case of shrimps, they have
a defined migration pattern related to their reproductive
cycle. The greatest differences are in the preferred habitats
Fig. 4 Biotransference and Pb
concentrations in AEPL
ecosystem components.
Concentrations within symbols
are mean concentrations (mg/
kg) and numbers on lines are
transference factors. For
sediments, numbers within
parentheses include bioavailable
metal concentration
592 Arch Environ Contam Toxicol (2008) 54:584–596
123
of postlarvae, juveniles, and adults: whether they are pre-
dominantly estuarine, inshore, or offshore and whether
demersal or pelagic (Dall et al. 1990). In the particular case
of nursery grounds for postlarval and juvenile stages of the
studied species, they spend part of their life cycle in
inshore areas, such as estuaries or coastal lagoon waters. At
the end of the period in the nursery grounds, juvenile
shrimps migrate offshore, usually to deeper water—a
migration that might involve a considerable longshore
movement.
Multidimensional scaling shown in Figure 6 displayed a
stress value of 0.10, indicating that metal concentrations
among individuals of the same species were similar.
Additionally, MDS ordination revealed two main groups:
Group B, including filter-feeders, was different from group
A, which included all other species. It clearly indicates that
Cd, Pb, and Zn concentrations in the two filter-feeders are
notably different from metal concentrations in
invertebrates, plants, sources, fish, and birds. The consum-
ers that eat larger fish would have higher exposure to
mercury than those that eat smaller fish (Burger et al. 2001);
similarly, Chen et al. (2000) provided field evidence of Zn
and mercury biomagnification from plankton to macro-
zooplankton and to fish. Thus, the fish Lutjanus colorado
and Cynoscion xanthulus, which eat fish, would be exposed
to relatively higher Cd, Pb, and Zn loads, allowing bioac-
cumulation; similarly, the birds Pelecanus occidentalis and
Phalacrocorax brasilianus, which also consume fish, tend
to accumulate comparable levels of the analyzed metals.
Considering that these fish species use or reside temporally
in the lagoon, it is probable that they reflect the food web of
the northeastern Pacific ocean (or the Gulf of California) but
not of lagoon. Upwelling events are characteristics in this
region, where the highest Cd levels could be expected and
fast and easy assimilation of dissolved Cd by primary pro-
ducers, and then by secondary producers.
Fig. 5 Biotransference and Zn
concentrations in AEPL
ecosystem components.
Concentrations within symbols
are mean concentrations (mg/
kg) and numbers on lines are
transference factors. For
sediments, numbers within
parentheses include bioavailable
metal concentration
Arch Environ Contam Toxicol (2008) 54:584–596 593
123
Species within trophic groups are primary producers
(group I), filter-feeders (group II), omnivores (group III),
detritivores (group IV), carnivores-secondary consumers
(group V), and carnivores-tertiary consumers (group VI)
separated differently to indicate that species of the same
trophic group shared similar metal concentrations (Fig. 6).
Separation of main groups A and B, evidenced by MDS
ordination, were not similarly grouped in the classification
analysis (Fig. 7). In the species classification, certain
coincidence among primary producers and tertiary carni-
vores was verified, which is difficult to explain. Filter-
feeder species were shown to group distinctly from other
species at greater that 95% similarity, indicating that they
shared similar metal concentrations. Carnivores of tertiary
level were also clearly separated from other species, with
the exception of Pelecanus occidentalis, which showed a
similar coordinate to primary producers. The shrimp Li-
topenaeus vannamei and Litopenaeus stylirostris exhibited
a clear separation and a behavior similar to the detritivore
fish species Mugil cephalus; this fish behaves similarly to
mangrove species, Rhizophora mangle, and Laguncularia
racemosa, which probably indicates that the main source of
M. cephalus is related to these mangroves.
Conclusions
In this study, Cd, Pb, and Zn concentrations were deter-
mined in a food web representative of the Altata-Ensenada
del Pabellon subtropical lagoon. Considering the feeding
habits, the 15 species examined were divided into 6 groups:
primary producers (6), detritivores (1), filter-feeders (2),
omnivores (2), and secondary (2) and tertiary (2) carni-
vores. The samples were collected from three nearby sites
where such groups of organisms reside a part or their whole
life cycle. The range of found concentrations was as fol-
lows: for primary producers, 0.10–0.87, 0.9–4.9, and 8.7–
117 mg/kg of Cd, Pb, and Zn, respectively; for detritivores,
0.1–0.3, 0.8–1.1, and 11–21 mg/kg for Cd, Pb, and Zn,
respectively; for filter feeders, 1.1–7.2, 2.1–3.4, and 1210–
1420 mg/kg for Cd, Pb, and Zn, respectively; for omni-
vores, 0.5–3.1, 0.5–0.9, and 53–61 mg/kg for Cd, Pb, and
Zn, respectively; for secondary carnivores, 0.2–0.9, 1.3–
2.6, and 17–22 mg/kg for Cd, Pb, and Zn, respectively; and
for tertiary carnivores, 0.7–1.2, 1.7–4.2, and 23–35 mg/kg
for Cd, Pb, and Zn, respectively.
Cadmium magnification was found partially (64.5% of
the different trophic links) in the lagoon ecosystem,
resulting in increased Cd concentrations in the muscle of
the cormorant Phalacrocorax. brasilianus. The mangrove
oyster Crassostrea corteziensis was the species in which
more elevated concentrations were found and in which
transference factors were relatively elevated, which might
be interpreted as evidence of Cd biomagnification in oys-
ters. Zn showed some evidence of biomagnification.
Positive biotransference (TF [ 1) from food sources to
consumers occurred in 58.1% of the trophic interactions
examined. Most of the TF [ 1 were associated to the low
Fig. 6 MDS ordination
showing grouping of AEPL
ecosystem species based on
mean concentrations of Cd, Pb,
and Zn. C. centralis, CCE;
Gracilaria sp., GS;
Polisyphonia sp., PS; R.mangle, RM; A. germinans, AG;
L. racemosa, LR; C.corteziensis, CCO; B. eburneus,
BE; L. stylirostris, LS; L.vannamei, LV; M. cephalus,
MC; L. colorado, LC; C.xanthulus, CX; P. occidentalis,
POC; P. brasilianus, POL
594 Arch Environ Contam Toxicol (2008) 54:584–596
123
trophic levels. All increases in mean Zn concentration were
those in which the filter-feeders mangrove oyster (Cras-
sostrea corteziensis) and barnacles (Balanus eburneus)
were involved. There were no systematic trends in the
magnitude of biotransference factors between low and high
trophic groups, which mighr be interpreted as insufficient
evidence of Zn biomagnification. From the number of
potential trophic interactions with TF [ 1 (45.2%), Pb was
comparatively less likely to be biomagnified. The highest
transference rates were observed in the link between preys
(white shrimp and mullet) and the pelican Pelecanus
occidentalis.
Acknowledgments The authors thank A. Nunez-Pasten (field
work), J. Salgado-Barragan (barnacle identification), S. Rendon-
Rodrıguez (shrimp identification), F. Silva (fish identification), B.
Mejıa (bird identification), C. Ramırez-Jauregui (bibliographic sup-
port), G. Ramırez-Resendiz (statistical analyses), C. Suarez-Gutierrez
(computing assistance), and H. Bojorquez-Leyva (laboratory
assistance).
References
Altschuler ZS (1980) The geochemistry of trace elements in marine
phosphorites, part 1. Characteristic abundances and enrichment.
In: Bentor YK (ed) Marine phosphorites: Geochemistry, occur-
rence, genesis. Society of Economic Paleontologists and
Mineralogists, Special Publication No. 29, Tulsa, pp 19–30
Amiard JC, Amiard-Triquet C, Metayer C (1985) Experimental study
of bioaccumulation, toxicity and regulation of some trace metals
in various estuarine and coastal organisms. Symp Biol Hung
29:313–323
Amiard JC, Amiard-Triquet C, Metayer C, Marchand J, Ferre R
(1980) Study on the transfer of Cd, Pb, Cu and Zn in neritic and
estuarine trophic chains. I. The inner estuary of the Loire
(France) in the summer of 1978. Water Res 14:665–673
Bargagli R (1998) Cadmium in marine organisms from the Tyrrhe-
nian sea: no evidence of pollution or biomagnification. Oebalia
19:13–25
Barwick M, Maher W (2003) Biotransference and biomagnification of
selenium, copper, cadmium, zinc, arsenic and lead in a temperate
seagrass ecosystem from Lake Macquarie Estuary, NSW,
Australia. Marine Environ Res 56:471–502
Biddinger GR, Gloss SG (1984) The importance of trophic transfer in
the bioaccumulation of chemical contaminants in aquatic
ecosystems. Residue Rev 9:104–145
Bowen HJM (1966) Trace elements in biochemistry. Academic Press,
New York
Burger J, Gaines KF, Boring CS, Stephens WL, Snodgrass J,
Gochfeld M (2001) Mercury and selenium in fish from the
Savannah River: species, trophic level, and locational differ-
ences. Environ Res 87:108–118
Calderon-Rodrıguez A (2005) Metales pesados en aves (patos y
cercetas) residentes y migratorias recolectadas en sistemas
lagunares del centro y sur de Sinaloa. Master Tesis. Posgrado
en Ciencias del Mar y Limnologıa, UNAM (in Spanish)
Carvalho FP, Fowler SW, Gonzalez-Farıas F, Mee LD, Readman JW
(1996) Agrochemical residues in the Altata-Ensenada del
Pabellon coastal lagoon (Sinaloa, Mexico): a need for integrated
coastal zone management. Int J Environ Health Res 6:209–220
Castilhos ZC, Bidone ED (2000) Hg biomagnification in the
ichthyofauna of the Tapajos river region, Amazonia, Brazil.
Bull Environ Contam Toxicol 64:693–700
Chen CY, Stemberger RS, Klaue B, Blum JD, Pickhardt PC, Folt CL
(2000) Accumulation of heavy metals in food web components
across a gradient of lakes. Limnol Oceanog 45:1525–1536
Dall W, Hill BJ, Rothlisberg PC, Sharples DJ (1990) The biology of
the Penaeidae. In: Blaxter JHS, Southward AJ (eds) Advances in
marine biology, Academic Press, San Diego
Delgadillo-Hinojosa F, Macıas-Zamora JV, Segovia-Zavala JA,
Torres-Valdes S (2001) Cadmium enrichment in the Gulf of
California. Marine Chem 75:109–122
Dethlefsen V (1978) Uptake, retention and loss of cadmium by brown
shrimp Crangon crangon. Meeresforschung 26:137–152
Dietz R, Riget F, Cleeman M, Aarkrog A, Johansen P, Hansen JC
(2000) Comparison of contaminants from different trophic levels
and ecosystems. Sci Total Environ 245:221–231
Edwards RRC (1978) Ecology of a coastal lagoon complex in
Mexico. Estuar Coastal Marine Sci 6:75–92
Forstner U, Wittmann GTW (1979) Metal pollution in the aquatic
environment. Springer-Verlag, Berlin Heidelberg, 485 pp
George MD, Kureishy TW (1979) Trace metals in zooplankton from
the Bay of Bengal. Indian J Marine Sci 8:190–192
Gray JS (2002) Biomagnification in marine systems: the perspective
of an ecologist. Marine Pollut Bull 45:46–52
Green-Ruiz C, Paez-Osuna F (2001) Heavy metal anomalies in
lagoon sediments related to intensive agriculture in Altata-
Ensenada del Pabellon coastal system (SE Gulf of California).
Environ Int 26:265–273
Guhathakurta H, Kaviraj A (2000) Heavy metal concentration in
water, sediment, shrimp (Penaeus monodon) and mullet (Lizaparsia) in some brackish water ponds of Sunderban, India.
Marine Pollut Bull 40:914–920
Hamer KC, Schreiber EA, Burger J (2002) Breeding biology, life
histories, and life history-environment interactions in seabirds.
In: Schreiber EA, Burger J (eds) Biology of marine birds. CRC
Press, Boca Raton, FL
Fig. 7 Classification of AEPL ecosystem species, based on similar-
ities between Cd, Pb, and Zn concentrations. C. centralis, CCE;
Gracilaria sp., GS; Polisyphonia sp., PS; R. mangle, RM; A.germinans, AG; L. racemosa, LR; C. corteziensis, CCO; B. eburneus,
BE; L. stylirostris, LS; L. vannamei, LV; M. cephalus, MC; L.colorado, LC; C. xanthulus, CX; P. occidentalis, POC; P. brasilianus,
POL
Arch Environ Contam Toxicol (2008) 54:584–596 595
123
IAEA (1987) Intercalibration of analytical methods on marine
environmental samples. Trace element measurements on fish
homogenate. Results of the Worldwide Intercomparison Run
MA-B-3/TM. Report No. 36. International Atomic Energy
Agency, Monaco
Mackay D, Fraser A (2000) Bioaccumulation of persistent organic
chemicals: mechanisms and models. Environ Pollut 110:375–
391
Mejıa-Sarmiento B (2001) La Acuacultura y las aves. In: Paez-Osuna
F (ed) Camaronicultura y medio ambiente. UNAM y El Colegio
de Sinaloa, Mexico (in Spanish)
Mendez L, Acosta B, Palacios E, Magallon F (1997) Effect of
stocking densities on trace metal concentration in three tissues of
the brown shrimp Penaeus californiensis. Aquaculture 156:21–
34
MESL (1997) (Marine Environmental Studies Laboratory) (1997)
Standard Operating Procedures. International Atomic Energy
Agency, Inorganic Laboratory. Monaco
Moody JR, Lindstrom RN (1977) Selection and cleaning of plastic
containers for storage of trace element samples. Anal Chem
49:2264–2267
Moriarty DJW (1976) Quantitative studies on bacteria and algae in
the food of the mullet Mugil cephalus L. and the prawn
Metapenaeus bennettae (Racek and Dall). J Exp Biol Ecol
22:131–143
NAS (1980) The international mussel watch. National Academy of
Sciences, Washington, DC
Nieboer E, Richardson DHS (1980) The replacement of the nonde-
script term ‘‘heavy metals’’ by a biologically and chemically
significant classification of metal ions. Environ Pollut 1:3–26
NIST (National Institute of Standards, Technology) (2000) Certificate
of analysis. Standard Reference Material 2977, mussel tissue.
NIST, Gaithersburg, MD
Otero N, Vitoria L, Soler A, Canals A (2005) Fertiliser character-
isation: major, trace and rare earth elements. Appl Geochem
20:1473–1488
Paez-Osuna F, Marmolejo-Rivas C (1990) Trace metals in tropical
coastal lagoon bivalves: Crassostrea corteziensis. Bull Environ
Contam Toxicol 45:538–544
Paez-Osuna F, Osuna-Lopez JI, Izaguirre-Fierro G, Zazueta-Padilla
HM (1993a) Heavy metals in clams from a subtropical coastal
lagoon associated with an agricultural drainage basin. Bull
Environ Contam Toxicol 50:915–921
Paez-Osuna F, Osuna-Lopez JI, Izaguirre-Fierro G, Zazueta-Padilla
HM (1993b) Heavy metals in oysters from a subtropical coastal
lagoon associated with an agricultural drainage basin. Bull
Environ Contam Toxicol 50:696–702
Paez-Osuna F, Ruiz-Fernandez AC, Botello AV et al (2002)
Concentrations of selected trace metals (Cu, Pb, Zn), organochl-
orines (PCBs, HCB) and total PAHs in mangrove oysters from
the Pacific coast of Mexico: an overview. Marine Pollut Bull
44:1303–1308
Phillips DJH, Rainbow PS (1988) Barnacles and mussels as
biomonitors of trace elements: a comparative study. Marine
Ecol Prog Series 49:83–93
Pielou EC (1975) Ecological diversity. Wiley, New York
Rainbow PS (1985) Accumulation of Zn, Cu and Cd by crabs and
barnacles. Estuar Coast Shelf Sci 21:669–686
Rainbow PS (1993) Biomonitoring of marine heavy metal pollution
and its application in Hong Kong waters. In: Morton B (ed) The
marine biology of the South China Sea, Proceedings of the first
international conference on the marine biology of Hong Kong
and the South China Sea. Hong Kong University Press, Hong
Kong, pp 235–250
Rainbow PS, Phillips DJH (1993) Cosmopolitan biomonitors of trace
metals. Marine Pollut Bull 26:593–601
Rainbow PS, Zongguo H, Songkai Y, Smith BD (1993) Barnacles as
biomonitors of trace metals in the coastal waters near Xiamen,
China. Asian Marine Biol 10:109–121
Rodrıgues-dos Santos I,Vieira-Silva-Filho E, Schaefer C et al (2006)
Baseline mercury and zinc concentrations in terrestrial and
coastal organisms of Admiralty Bay, Antarctica. Environ Pollut
140:304–311
Ruelas-Inzunza J, Paez-Osuna F (1998) Barnacles as biomonitors of
heavy metal pollution in the coastal waters of Mazatlan harbour
(Mexico). Bull Environ Contam Toxicol 61:608–615
Ruelas-Inzunza J, Paez-Osuna F (2004a) Distribution and concentra-
tion of trace metals in tissues of three penaeid shrimps from
Altata-Ensenada del Pabellon lagoon (SE Gulf of California).
Bull Environ Contam Toxicol 72:452–459
Ruelas-Inzunza J, Paez-Osuna F (2004b) Trace metals in tissues of
resident and migratory birds from a lagoon associated to an
agricultural drainage basin (SE Gulf of California). Arch
Environ Contam Toxicol 47:117–125
Ruelas-Inzunza J, Paez-Osuna F (2006) Trace metal concentrations in
different primary producers from Altata-Ensenada del Pabellon
and Guaymas Bay (Gulf of California). Bull Environ Contam
Toxicol 76:327–333
Ruiz-Nieto IC (2005) Habitos alimenticios de Hoplagrus guentherii,Lutjanus argentiventris, L. colorado, L. guttatus, L. novemfas-ciatus, L. peru (Pisces: Lutjanidae) presentes en las costas del
Centro del Sur de Sinaloa. Tesis de Maestrıa, Posgrado en
Ciencias del Mar y Limnologıa. UNAM (in Spanish)
Szefer P (1991) Interphase and trophic relationships of metals in a
southern Baltic ecosystem. Sci Total Environ 101:201–215
Szefer P (1998) Distribution and behaviour of selected heavy metals
and other elements in various components of the southern Baltic
ecosystem. Appl Geochem 13:287–292
Szefer P, Skwarzec B, Koszteyn J (1985) The occurrence of some
metals in mesozooplankton taken from the Southern Baltic.
Marine Chem 17:237–253
Timmermans KR, Van Hattum B, Kraak MHS, Davids C (1989)
Trace metals in a littoral food web: concentrations in organisms,
sediment and water. Sci Total Environ 87/88:477–494
Wang W-X, Fisher NS, Luoma SN (1996) Kinetic determinations of
trace element bioaccumulation in the mussel Mytilus edulis.
Marine Ecol Prog Series 140:91–113
Zar JH (1984) Biostatistical analysis. Prentice Hall, Englewood
Cliffs, NJ
Zeisler R, Becker DA, Gills TE (1995) Certifying the chemical
composition of a biological material: a case study. Fresnius J
Anal Chem 352:111–115
596 Arch Environ Contam Toxicol (2008) 54:584–596
123