Baseline
Edited by Bruce J. Richardson
The objective of BASELINE is to publish short communications on different aspects of pollution of the marine
environment. Only those papers which clearly identify the quality of the data will be considered for publication.
Contributors to Baseline should refer to ‘Baseline—The New Format and Content’ (Mar. Pollut. Bull. 42, 703–704).
Dynamics of trace metal concentrations in an intertidal rockyshore food chain
Wen-Xiong Wang *, Pan Wong
Department of Biology, The Hong Kong University of Science and Technology (HKUST), Clear Water Bay, Kowloon, Hong Kong
Numerous studies have measured the concentrations ofvarious trace metals in marine organisms (for a review seeEisler, 1981; Neff, 2002), often in response to concernsabout trace metal contamination in seafood or in anattempt to employ marine organisms as biological moni-tors of coastal contamination. In these studies, marineorganisms are typically collected from polluted and unpol-luted environments and their concentrations of metals arequantified. The main objectives of these studies are toexamine whether the organisms are contaminated withthe metals and whether there are any spatial or temporaltrends in metal contamination in the coastal or estuarineenvironment. Few studies have attempted to mechanisti-cally interpret the metal body concentrations in these ani-mals (Langston and Spence, 1995; Wang et al., 1996;Blackmore, 2000; Rainbow, 2002; Luoma and Rainbow,2005). Over the past decade, the development of kineticmodeling has rekindled interest in the mechanistic interpre-tation of metal concentrations in marine invertebrates. Inaddition, a few studies have also attempted to addresspotential trophic interactions in accounting for the vari-ability of trace metal concentrations in predators (Black-more, 2000, 2001; Blackmore and Morton, 2002).
Trophic transfer has increasingly been recognized as animportant pathway for metal accumulation in marineinvertebrates (Wang and Fisher, 1999; Wang, 2002). Bio-
magnification occurs when the metals are transportedthrough a food chain at increasing concentrations in theanimals at higher trophic levels. Metal biomagnificationhas long been recognized as occurring with Hg (mainly inits methylated form, methylmercury) and cesium (Wang,2002). Evidence has largely come from measurements infish or other higher level organisms (e.g., birds, ducks).
There have been fewer studies of intertidal rocky shorefood chains. Several studies have found that metal concen-trations in predatory snails from intertidal rocky shoreswere unusually high (Blackmore, 2000; Jeng et al., 2000).There is thus considerable interest in examining the trophicinteraction and any metal biomagnification in such foodchains. Intertidal rocky shores host diverse species of inver-tebrates that differ tremendously in their metal accumula-tion patterns and thus metal concentrations, even amongthe closely related species such as bivalves (e.g., musselsand oysters).
In this study, the concentrations of five trace metals/metalloids (Ag, Cd, Cu, Se, and Zn) were measuredmonthly for one year in a predator-prey chain on an inter-tidal rocky shore in Hong Kong. The relationships amongmetals, species and seasons were investigated, with specialemphasis on potential biomagnification of metals in thetop predator. The animals were collected from a rockyshore in Clear Water Bay, where the dominant prey speciesincluded the black mussels Septifer virgatus, the oyster Sac-
costrea cucullata, and the barnacle Tetraclita japonica; thepredators included the snail Morula musiva. Another toppredator typical of such rocky shores is the starfish, which
* Corresponding author. Tel.: +852 23587346; fax: +852 23581559.E-mail address: [email protected] (W.-X. Wang).
www.elsevier.com/locate/marpolbul
Marine Pollution Bulletin 52 (2006) 332–356
was only occasionally observed in this area. Clear WaterBay is in the eastern part of Hong Kong and subjected tosignificant influence from ocean currents. The bay can beconsidered relatively pristine, without significant impactfrom anthropogenic activity. The salinity of the bay israther constant throughout the different seasons (typically25–32 ppt).
The invertebrates were collected from an exposed shorein a rocky area. All species except the oyster S. cucullata
were collected from June 2003 to June 2004. The oysterswere collected from July 2003 to June 2004. For the barna-cles, five bodies were combined into one sample, becausethe mass of an individual organism was too small for metalanalysis. For the other species, 6–8 replicate individuals ofsimilar body sizes were sampled each month. The sampleswere collected randomly from the site, then placed in poly-thene bags and frozen at �20 �C until metal analysis.
In the laboratory, the animals were dissected usingstainless steel knives and briefly rinsed with nanopure dis-tilled water. The bodies were dried at 60 �C in an acid-cleaned test tube. The dry mass of each replicate wasmeasured after the mass had reached a constant weight.Concentrated HNO3 was added and digestion was per-formed in a heating block. The digests were then dilutedwith nanopure distilled water for metal analysis. Thedigests were analyzed for Ag, Cd, Cu, Se, and Zn usinginductively coupled plasma mass spectrometry (ICP-MS)(Perkin–Elmer, Elan 6000). Further dilution was madefor the Cu and Zn measurements, since the concentrationof the samples was too high for the ICP-MS. Throughoutthe metal analysis, oyster standards (Standard ReferenceMaterial 1566 Oyster tissue, National Institute of Stan-dards and Technology, Gaithersburg, MD) were used forchecking the methodology. Comparisons of measurementsperformed on the standards with their certified values areshown in Table 1. Recoveries were 90–110% for Cd, Cu,Se, and Zn. For Ag, the recovery was somewhat lower,i.e., 83%. All the metal concentrations were expressedbased on the dry weights of tissues.
Over the one-year sampling period, the tissue dryweights of the mussels and oysters were much lower duringAugust–November period than during the winter season,which is likely caused by the reproductive cycle of thesebivalves (Fig. 1). The dry weights of the barnacles were alsolower in the summer season (July–September) than duringthe other seasons, again probably caused by reproduction.
There was no clear pattern of tissue dry weight for thesnails through the seasons. It should be noted that only6–8 replicates were collected at each sampling time, andefforts were made to select comparable body sizes in eachmonthly sampling.
The metal concentrations were first correlated with thetissue dry weight of the animals using an allometric powerfunction (Boyden, 1974, 1977). Significant correlationsbetween metal concentration and tissue dry weight werefound for Ag, Cd, and Zn in the mussels, and Ag and Znin the oysters (Table 2). No significant correlation wasfound for the barnacles or snails, presumably because thebody tissue weights were within a narrow range (0.16–0.4 g for each composite of five individual barnacles, and0.10–0.21 g for snails) throughout the different seasons.Interestingly, the allometric coefficients for Cd and Zn inthe two bivalves were �0.20 to �0.28, whereas they weremuch higher for Ag (�0.575 to �0.676), indicating a higherdependence of Ag concentration on body size in bivalves.Numerous studies have measured the size dependence ofmetal concentrations in such bivalves, but often over amuch wider range of body sizes (Boyden, 1977; Wang
Table 1Comparison of the certified metal concentrations in the oyster standardreference and the measured values (lg g�1)
Certified values ± std Measured values ± std % Recovery
Ag 0.666 ± 0.009 0.554 ± 0.077 83.1Cd 2.48 ± 0.08 2.233 ± 0.079 90.0Cu 71.6 ± 1.6 67.2 ± 2.3 93.8Se 2.06 ± 0.15 2.27 ± 0.32 110Zn 1424 ± 46 1405 ± 97 98.7
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Fig. 1. Seasonal variations in tissue dry weight of the collected inverte-brates. For barnacles, each measurement represents five bodies. Mean ±SD (n = 6–8).
Table 2Size allometric coefficients (b) of metal concentrations in the black musselSeptifer virgatus and the rock oyster Saccostrea cucullata
Septifer virgatus Saccostrea cucullata
b r2 b r2
Ag �0.676 0.235*** �0.575 0.277***
Cd �0.272 0.155*** NSCu NS NSSe NS NSZn �0.202 0.131** �0.239 0.174***
r2: Correlation coefficient. No relationship was found for the barnaclesand snails. NS: not significant.** Significant at the p < 0.01 level.
*** Significant at the p < 0.001 level.
Baseline / Marine Pollution Bulletin 52 (2006) 332–356 333
and Fisher, 1997). Very different power coefficients havebeen found in these studies.
To avoid any inherent influence of body size on tracemetal concentrations, all the body concentrations in mus-sels and oysters were standardized to 0.4 g and 0.3 g,respectively, using the allometric coefficients (with signifi-cant correlations only) before the analysis of the seasonalvariations. For barnacles and snails, no such standardiza-tion was made. Fig. 2 shows the seasonal variations inthe concentrations of the five metals in S. virgatus, S. cucul-
lata, T. japonica, and M. musiva. Generally, metal concen-trations varied significantly through the seasons (one-wayANOVA, p < 0.001 for all metals and species, except Znin snails (p < 0.01), Cu in oysters (p < 0.05), and Zn in bar-nacles (p < 0.05)). The only exception was Cu in the snails,which was not significantly influenced by the season(p > 0.05, one-way ANOVA). However, there was no con-sistent pattern for most of the metals with regard to sea-sonal variation. For the three prey species, it appears thatthe concentrations in the summer (June and July) werelower than those in other seasons, likely caused by thereproduction of the animals or the very low phytoplanktonbiomass present during the summer.
Ag concentrations in the black mussels were much lowerthan in the other three species, with typical concentrationsof 0.01–0.06 lg g�1. Concentrations in the oysters (0.7–2.8 lg g�1) were higher than those in the barnacles (0.6–1.4 lg g�1). The predators contained the highest Agconcentrations (e.g., as high as 10 lg g�1 during October
and December). Cd concentrations in the three prey specieswere rather comparable (1.5–5.0 lg g�1), but were highestin the snails (e.g., 11.7 lg g�1 in August). For Cu, oystersand snails contained the highest concentrations, both inthe range 300–880 lg g�1, whereas Cu concentrations werelowest in the barnacles. The concentrations of Se in themussels and oysters were comparable (1.6–3.8 lg g�1),and its concentration in the snails was the highest (6.7–15 lg g�1). Similar to Cu, the concentrations of Zn in theoysters and snails were the highest (630–3080 lg g�1), butthe barnacles also contained very high Zn concentrationsin their bodies (820–1200 lg g�1). The concentration ofZn in the mussels was the lowest among the four species(53–108 lg g�1).
The data show striking differences in the metal bodyconcentrations in different species of marine invertebrates,even among the taxonomically close species. It is interest-ing to note the very low Ag concentrations in the blackmussels (0.01–0.06 lg g�1). Such low values are in strongcontrast to Ag concentrations measured in the commonmussel Mytilus edulis collected from different regions ofUS coastal waters (geometric mean of 0.17lg g�1, O�Con-nor, 1992). Ng and Wang (2005) measured Ag concentra-tions in the green mussel Perna viridis collected fromcoastal (Eastern) and estuarine (Western) sites in HongKong. The Ag concentrations in the estuarine populationwere 0.04–0.17lg g�1, but much higher concentrationswere found in the coastal population (0.21–0.28lg g�1).The lower Ag concentration was attributed to higher Agefflux from the mussels collected from the estuarine site.It would be interesting to examine the mechanisms under-lying such very low Ag concentrations in black mussels.There were also major differences between the black mus-sels and the oysters. For example, the concentrations ofclass B type or borderline metals (Ag, Cu, Cd, Zn) in theoysters were higher than those in the mussels, whereas theirconcentrations of Se were comparable. A similar patternhas been consistently observed in the National Status andTrends program which uses mussels (Mytilus sp.) andAmerican oysters (Crassostrea virginica) to monitor coastalcontamination in the US (O�Connor, 1992).
The barnacles had the lowest Cu concentrations amongthe four species of invertebrates, but their Se and Zn con-centrations were very high. These data strongly suggestedthat it is difficult to discern any trend in metal concentra-tions across metals and animals. An important task is thusto mechanistically interpret the accumulated data on theconcentrations of metals in these animals (Luoma andRainbow, 2005). Among the five metals examined, thegreatest differences in metal concentrations among differentspecies were found for Cu and Zn, which varied by 50–130times and 15–32 times, respectively. The high Zn concen-trations in the barnacles and oysters were mainly causedby their very efficient dietary assimilation, as well as bythe exceedingly low rate of Zn efflux from these animals(Wang et al., 1999; Ke and Wang, 2001). Wang et al.(1999) were able to predict the phenomenal Zn concentra-
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Fig. 2. Seasonal variations of metal concentrations in collected inverte-brates. For mussels and oysters, the tissue metal concentrations werestandardized to body weights of 0.4 g and 0.3 g, respectively. Mean ± SD(n = 6–8).
334 Baseline / Marine Pollution Bulletin 52 (2006) 332–356
tions observed in the barnacle Balanus amphitrite using akinetic model. Similarly, a kinetic model was able to pre-dict the Zn concentrations in oysters with a high dietaryZn assimilation and low Zn efflux (Ke and Wang, 2001).In contrast to barnacles and oysters, the assimilation effi-ciency of Zn in mussels is generally lower, and its effluxmuch more rapid (by an order of magnitude), both ofwhich contribute to the low Zn concentrations seen in mus-sels (Chong and Wang, 2001). No biokinetic data are avail-able for Cu in the four species of invertebrate studied here.
The concentrations of Ag, Cd, and Se were consistentlyhigher in the snails than in any of the prey species, suggest-ing that these metals have a high potential for biomagnifi-cation during their transfer to the top predator. Theconcentrations of Cu and Zn in the predators were compa-rable to those measured in the prey (oysters and barnacles),thus the potential biomagnification of these two metals wasdependent on the choice of prey. It would be difficult toconclude that Cu and Zn are biomagnified without knowl-edge on the specific prey that the predators ingest. Wang(2002) discussed possible mechanisms underlying thepotential biomagnification of metals during trophic trans-fer, including high dietary assimilation and low efflux rateconstants, even in cases where the ingestion rate of thepredatory animals is low. A few recent studies have demon-strated that dietary metal assimilation efficiencies (AEs) inthe predatory whelk Thais clavigera are exceedingly high(53–94%) when the whelks are feeding on different preyspecies (Blackmore and Wang, 2004; Cheung and Wang,2005). Cheung and Wang (2005) further showed that theAEs of Ag, Cd and Zn from barnacle prey were lower thanfrom other prey (mussels, limpets, oysters and herbivoroussnails), especially for Zn.
Questions therefore remain whether predatory snails canact as a good biomonitor of metal contamination in coastalenvironments. Ideally there should be a linear relationshipbetween bioavailable metal concentrations in the environ-ment and metal concentrations in the biomonitor. Forthe predators, this condition may be difficult to meet, espe-cially if trophic transfer instead of dissolved exposure is thepredominant route by which the metals enter into the pred-ator (Wang and Ke, 2002; Blackmore and Wang, 2004). Inaddition, given the complicated internal metal processingby the predators, metals in the predator may not readilyreflect metals in the prey, especially for metals that maybe regulated by the animals (e.g., Cu, Zn, see below).
Since several metal concentrations were simultaneouslyquantified in the same individuals, correlations were soughtamong the different metals (Table 3). Among the three fil-ter-feeders, significant correlations were observed for Cdvs. Zn, and Ag vs. Cu. For other metals, correlations werealso observed (e.g., Cd vs. Se in oysters, and Ag and Cdwith other metals in barnacles). Such correlations mayreflect the metals� chemical similarity or the animals� han-dling strategies. For example, the Cd and Zn uptake ratesin marine invertebrates are often coupled, especially whendietary assimilation and dissolved uptake are considered
together (Wang and Dei, 1999; Chong and Wang, 2001).There have been very few studies on the interaction ofAg and Cu in marine animals, but Cu uptake from the dis-solved phase may be dominated by Cu+, which may behavesimilarly with Ag+. Clearly, it is necessary to further studythe interaction of metals in these animals. For snails, it isdifficult to discern any pattern based on the chemical prop-erties of the metals, probably because these animals mayhave regulated some of the metals, and any difference inmetal chemistry can be confounded during transferthrough the food chain.
Correlations were also sought among the different filter-feeders (Table 4). Significant correlations were documentedonly for Cd and Zn between the mussels and oysters, andfor Se and Zn between the mussels and barnacles. Therewas no correlation for any of the metals between oystersand barnacles. Such correlations may be caused by similaruptake pathways or dietary food sources. Both mussels andoysters are suspension feeders, and their food includes
Table 3Correlation coefficients (r2) among the concentrations of different metalswithin a single species of invertebrate
Cd Cu Se Zn
Mussels
Ag NS 0.180*** NS NSCd 1.000 NS NS 0.278***
Cu 1.000 NS NSSe 1.000 NS
Oysters
Ag NS 0.056* NS NSCd 1.000 NS 0.179** 0.115**
Cu 1.000 NS 0.155*
Se 1.000 NS
Barnacles
Ag 0.406*** 0.412*** 0.075* 0.290***
Cd 1.000 0.208*** 0.332*** 0.203***
Cu 1.000 NS NSSe 1.000 0.075*
Snails
Ag NS NS 0.064* 0.100**
Cd 1.000 0.133** NS NSCu 1.000 NS 0.054*
Se 1.000 0.118**
NS: not significant.* Significant at p < 0.05.
** Significant at p < 0.01.*** Significant at p < 0.001.
Table 4Correlation coefficients (r2) of trace metal concentrations between filter-feeders
Ag Cd Cu Se Zn
Mussels vs. oysters NS 0.609** NS NS 0.440*
Mussels vs. barnacles NS NS NS 0.341* 0.329*
Oyster vs. barnacles NS NS NS NS NS
NS: not significant.* Significant at p < 0.05.
** Significant at p < 0.01.
Baseline / Marine Pollution Bulletin 52 (2006) 332–356 335
phytoplankton and other seston materials in the water col-umn. The feeding behavior of barnacles is more compli-cated (micro-filtering of small food materials andraptorial feeding on large food particles such aszooplankton).
Recently, it has been demonstrated that trophic transferis an important mechanism of overall metal bioaccumula-tion in marine invertebrates (Wang, 2002). Se is predomi-nantly accumulated from dietary sources in differentspecies of marine invertebrates. For predatory animals, die-tary accumulation also predominates in metal accumula-tion, primarily because of their exceedingly efficientassimilation of dietary metals and their low dissolveduptake from the water (Blackmore and Wang, 2004). Forsuspension feeders (e.g., mussels, oysters, barnacles), die-tary assimilation either dominates or is at least equallyimportant with aqueous uptake, largely resulting from themoderate assimilation and the rather high dissolved uptakein these animals (Wang and Fisher, 1999). Since dietaryuptake often dominates metal accumulation in marine pre-dators, metal concentrations in the predator may be corre-lated with the metal concentrations in the prey. However, inthis study, significant correlations between the predatorsand the prey species were found only for Cd in the oystersand mussels (Table 5). For Ag, the correlation was onlymarginal (p = 0.07–0.09). No significant correlation wasdocumented for Cu or Zn in the snails with any of the preyspecies. Se in the snails was also significantly correlated withits concentration in the barnacles, but for other metals, nosuch significant correlation was found in this species.
The diet of an organism is important in determining itsaccumulated metal concentrations (Langston and Spence,1995). Blackmore (2000) compared the concentrations ofCd, Cu, and Zn in a predatory snail T. clavigera fromtwo different locations where the diets varied. Thais col-lected from an exposed shore contained higher Zn bodyconcentrations due to the high Zn concentration in the bar-nacle prey (Tetraclita squamosa), whereas Thais collectedfrom a sheltered shore had higher Cu concentrations dueto the higher proportion of haemocyanin-containing gas-tropod prey (the limpet Siphonaria japonica) in the diet.This study demonstrated that differences in prey composi-tion can lead to different metal concentrations in predators.
Nevertheless, the results of this study did not show astrong correlation between prey and predator concentra-tions in different seasons. Several possible mechanisms
may explain this. First, the amount of each prey that thepredators consumed may vary through the seasons, andgiven the wide range of metal concentrations observed inthe prey, metal concentrations in the predator may notreflect average concentrations in the prey. It is most likelythat the body metals in the gastropods, for example, werederived from a mixture of different prey instead of singleprey. There are very few data available on the diet of pre-dators in the field (Blackmore, 2000). Second, gastropodsmay be able to regulate the levels of some of the metals(Cu and Zn) to maintain a relatively constant concentra-tion through the seasons. Indeed, the variation in Cu andZn concentrations observed in the predators were smallerthan those in the prey species. Third, metal concentrationsin the predators may not synchronize with those in the preybecause the predators may take a significantly long time toreach a steady-state concentration following the ingestionof different prey. Further laboratory experiments arerequired to test this hypothesis.
This study has demonstrated a high potential for the bio-magnification of Ag, Cd, and Se in an intertidal rocky shorefood chain. The concentrations of these metals (includingCu and Zn) in predatory gastropods were found to beexceedingly high, even in animals collected from a pristinemarine environment. Correlations were observed betweenmetals with similar uptake pathways within each prey spe-cies. The metal concentrations in the predators were notcoupled closely with the variations in metal concentrationin a single prey, likely as a result of differences in prey selec-tion and the handling of incoming metals in the predators.Rocky shore intertidal food chains contain marine organ-isms with very diverse strategies of metal handling, and pro-vide ample opportunity to study the complex interactionscontrolling metal trophic transfer in marine ecosystems.
Acknowledgement
This study was supported by a Competitive EarmarkedResearch Grant from the Hong Kong Research GrantsCouncil (HKUST6405M/05) to W.-X. Wang.
References
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Table 5Correlation coefficients (r2) of metal concentrations in the predatorygastropod Morula musiva with its potential prey
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Mussels 0.275 (p = 0.07) 0.429* NS 0.261 NSOysters 0.256 (p = 0.09) 0.564** NS NS NSBarnacles NS NS NS 0.358* NS
NS: not significant.* Significant at p < 0.05.
** Significant at p < 0.01.
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0025-326X/$ - see front matter � 2005 Elsevier Ltd. All rights reserved.
doi:10.1016/j.marpolbul.2005.10.023
Imposex in Hexaplex (Trunculariopsis) trunculus(Gastropoda: Muricidae) from the Ria Formosa lagoon
(Algarve coast—southern Portugal)
P. Vasconcelos a,*, M.B. Gaspar a, M. Castro b
a Instituto Nacional de Investigacao Agraria e das Pescas (INIAP/IPIMAR), Centro Regional de Investigacao Pesqueira do Sul (CRIPSul),
Avenida 5 de Outubro s/n, P-8700-305 Olhao, Portugalb Centro de Ciencias do Mar (CCMAR), Universidade do Algarve (UAlg), P-8005-139 Faro, Portugal
The phenomenon known as imposex (Smith, 1971) orpseudohermaphroditism (Jenner, 1979) is the developmentand superimposition of male secondary sex characters(penis and vas deferens) onto females of prosobranch gas-tropods, resulting ultimately in sterile females and repro-ductive failure. This apparently irreversible abnormalityis a morphological indicator of sub-lethal exposure toorganotin compounds, namely tributyltin (TBT) and itsderivative compounds, extensively applied as biocides inantifouling paints for boats and ships hulls (Terlizziet al., 2001).
Imposex is a widespread phenomenon that affectsseveral coastal gastropod species, and more recently, alsooffshore gastropods (Ellis and Pattisina, 1990). At ambient
concentrations of few nanograms per litre, TBT potentiallyinduces genital abnormalities in several marine gastropodspecies, affecting at least 63 genera and 118 species (Fioroniet al., 1991). For these reasons, the use of morphologicalparameters in imposex-affected gastropod species has beenwidely used to assess coastal and offshore TBT pollution.
Some studies have been undertaken on imposex inHexaplex (Trunculariopsis) trunculus, mostly in the Medi-terranean including Spain (El Hamdani et al., 1998),France (Martoja and Bouquegneau, 1988), Italy (Terlizzi,2000; Terlizzi et al., 1997, 1998, 1999, 2004; Chiavariniet al., 2003; Pellizzato et al., 2004), Malta (Axiak et al.,1995, 2000, 2003) and Israel (Rilov et al., 2000). T. truncu-lus has proved to be a good sentinel species for TBTbiomonitoring in coastal waters, being considered one ofthe most sensitive neogastropod species to TBT contamina-tion, exhibiting initial stages of imposex at concentrations
* Corresponding author. Tel.: +351 289 700500; fax: +351 289 700535.E-mail address: [email protected] (P. Vasconcelos).
Baseline / Marine Pollution Bulletin 52 (2006) 332–356 337
