Trophic Distribution of Cd, Pb, and Zn in a Food Web from Altata-Ensenada del Pabellón Subtropical Lagoon, SE Gulf of California

Arch Environ Contam Toxicol (2008) 54:584–596 DOI 10.1007/s00244-007-9075-4

Trophic Distribution of Cd, Pb, and Zn in a Food Web from Altata-Ensenada del Pabello´n Subtropical Lagoon, SE Gulf of California J. Ruelas-Inzunza Æ F. Pa´ez-Osuna

Received: 14 August 2007 / Accepted: 22 October 2007 / Published online: 20 November 2007 Ó Springer Science+Business Media, LLC 2007

Abstract The aim of the work was to obtain a comparative view of the trophic distribution of Cd, Pb, and Zn in different organisms of the food web (from primary producers to top predators), considering representative species in Altata-Ensenada del Pabello´n 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 examination 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

J. Ruelas-Inzunza Technological Institute of Mazatla´n/Environmental Section, P.O. Box 757, Mazatla´n 82000, Sinaloa, Mexico F. Pa´ez-Osuna (&) Universidad Nacional Auto´noma de Me´xico, P.O. Box 811, Mazatla´n 82000, Sinaloa, Me´xico e-mail: [email protected]

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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 metals, several authors have reported biomagnification of selenium (Biddinger and Gloss 1984) and zinc (Timmermans 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 Pabello´n lagoon (AEPL) is moderately contaminated with Cd, Cu, Mn, Pb, and Zn (Ruelas-Inzunza and Pa´ez-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 agrochemicals are used (Carvalho et al. 1996), including fertilizers

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and fungicides containing metals. The utilization of phosphorus-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 elements 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 borderline. 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 biological 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 organisms themselves or to human consumers. In this study, specimens of different trophic levels (from primary producers 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 biomagnification 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 ordination 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

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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 Pabello´n (232 km2), (2) Altata (75 km2), and inner lagoons (Caimanero, 3 km2; Bataoto, 2 km2; and Chiricahueto, 23 km2). The two main regions are connected via a narrow channel where the Culiaca´n 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 (Caldero´n-Rodrı´guez 2005), fish (Edwards 1978; Moriarty 1976; RuizNieto 2005), and crustaceans (Dall et al. 1990; Edwards 1978). Considering the feeding habits, species were divided into several groups: primary producers, detritivores, filterfeeders, omnivores, and secondary and tertiary carnivores (Table 1). Most species were classified with sufficient confidence into specific trophic groups. However, an issue in developing 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 collection (i.e., mainly adults), the classification was made taking into account the predominant feeding habit. For example, in adult shrimps Litopenaeus vannamei and Litopenaeus 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 macroorganisms 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

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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

Autotrophic

Whole

\118 lm

–

–

2

A

Primary producers (sources) Phytoplankton

Coscinodiscus centralis

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

Crassostrea corteziensis Balanus eburneus

Filter-feeder Filter-feeder

Soft tissue Soft tissue

36–55 11–23

7.2–21.3 1.4–7.3

25 60

3 3

B B

Primary consumers Oysters Barnacles Shrimps Fish

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

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

Pelecanus occidentalis

Carnivorous

Muscle

850–910

3500–3900

1

2

C

Phalacrocorax brasilianus

Carnivorous

Muscle

470–550

889–1057

1

6

C

Tertiary consumers Birds

Note: See Figure 1 for sampling locations A, B, and C

samples were taken far away from any immediate local pollution sources; therefore, results could represent the average of metal concentrations in biota. Individuals of

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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

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(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 complete 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 Rainbow 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 leadfree ammunitions; a hunting permit from the official authority in environmental matters was obtained (permit SEMARNAT DOO.O2-3324) in order to collect the avifauna. Birds were placed in individual plastic bags and in similar manner all samples were placed on ice and transported 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 barnacles, 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 phytoplankton, 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 analysis, 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

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prevent contamination of samples (Moody and Lindstrom 1977). After taxonomic identification and determination of length and weight of specimens, dissection with a stainlesssteel 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 conditions given by MESL (1997).

Metal Analysis Analyses were made by flame atomic absorption spectrophotometry 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 absorption spectrophotometry was used. Samples replicates (n = 6) for each group of species and the different reference 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 IAEAMEL, 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 concentration data for the examined metals have been previously reported for penaeid shrimps (Ruelas-Inzunza and Pa´ez-Osuna 2004a), birds (Ruelas-Inzunza and Pa´ezOsuna 2004b), and primary producers (Ruelas-Inzunza and Pa´ez-Osuna 2006).

Data Analyses In order to have an idea of the degree of metal accumulation in the analyzed species with respect to their

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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 sediments (collected in 1991) were taken from Green-Ruiz and Pa´ez-Osuna (2001). Average concentrations of metals in the analyzed species 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 Kolmogorov–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 nonparametric analyses. Classification and ordination techniques were employed to examine groupings of species 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 concentrated high values of Cd is not abnormal; through

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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 mesozooplankton 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 (Me´ndez 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 Caldero´n-Rodrı´guez (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 (Pa´ez-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 Mazatla´n 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 Mazatla´n), Ruelas-Inzunza and Pa´ez-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 (Pa´ez-Osuna et al. 2002). As it was mentioned earlier, AEPL receives the discharge of untreated sewage from numerous towns and Culiaca´n city; additionally, agriculture and aquaculture effluents discharge in this water body. Early studies (Pa´ez-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

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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

Primary producers (sources)

Cd

Pb

0.24 ± 0.20a,b

2.3 ± 1.4

Zn 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 2.1 ± 3.0a

0.9 ± 0.3 1.6 ± 1.3

15.0 ± 0.6 494 ± 645

Primary consumers 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

0.6 ± 0.4

2.1 ± 1.2

18.1 ± 6.7

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

0.9 ± 0.3b

2.9 ± 1.8

29.1 ± 8.3 23.3 ± 5.0

Secondary consumers Fish Tertiary consumers Birds

P. occidentalis

POC

0.7 ± 0.1

4.2 ± 1.5

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

fungicides containing metals are applied. Green-Ruiz and Pa´ez-Osuna (2001), considering different criteria, examined 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%) concentrations of metals were associated with agricultural discharges and Culiaca´n River inputs. From these comparisons 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 California 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 shellfish, shrimp, fish, birds, barnacles, macroalgae, and mangroves as well as the different aquatic geochemistry of the trace metals affect the intake, assimilation, and subsequent 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 patterns; 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 correspondent concentrations in the dissolved and suspended fractions of the lagoon waters, Pa´ez-Osuna and MarmolejoRivas (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

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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

live near the lagoon and with short traveling distance (Lutjanus colorado and Cynoscion xanthulus). Furthermore, 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 (Mejı´a-Sarmiento 2001).

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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 macroalgae 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 magnitude 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 mangroves (Avicennia germinans; Laguncularia racemosa; Rhizophora mangle) to Litopenaeus stylirostris, to Cynoscion 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 concentrations 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 biomagnification, 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 biomagnification: (1) from mangroves (Laguncularia racemosa) to Litopenaeus stylirostris, to Cynoscion xanthulus, to Phalacrocorax brasilianus, to Lutjanus colorado; (2) from

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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

phytoplankton (Coscinodiscus centralis) and/or Polisyphonia 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 concluded that Pb is not biomagnified along the successive trophic levels of the food chain. Barwick and Maher (2003) found positive biotransference 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 magnitude 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

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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

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. Rodrı´gues-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

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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 Litopenaeus vannamei and Litopenaeus stylirostris and the two filter-feeders examined. Fish Lutjanus colorado and Cynoscion 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

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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

of postlarvae, juveniles, and adults: whether they are predominantly 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 consumers 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 macrozooplankton 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 bioaccumulation; 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 producers, and then by secondary producers.

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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 carnivores was verified, which is difficult to explain. Filterfeeder 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 Litopenaeus 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 determined in a food web representative of the Altata-Ensenada 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

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del Pabello´n 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) carnivores. 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 follows: 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 omnivores, 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 oysters. 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

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Fig. 7 Classification of AEPL ecosystem species, based on similarities 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

trophic levels. All increases in mean Zn concentration were those in which the filter-feeders mangrove oyster (Crassostrea 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. Nu´n˜ez-Paste´n (field work), J. Salgado-Barraga´n (barnacle identification), S. Rendo´nRodrı´guez (shrimp identification), F. Silva (fish identification), B. Mejı´a (bird identification), C. Ramı´rez-Ja´uregui (bibliographic support), G. Ramı´rez-Rese´ndiz (statistical analyses), C. Sua´rez-Gutie´rrez (computing assistance), and H. Bojo´rquez-Leyva (laboratory assistance).

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