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).

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