Dynamics of trace metal concentrations in an intertidal rocky shore food chain

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<ul><li><p>Baseline</p><p>Edited by Bruce J. Richardson</p><p>The objective of BASELINE is to publish short communications on different aspects of pollution of the marine</p><p>environment. Only those papers which clearly identify the quality of the data will be considered for publication.</p><p>Contributors to Baseline should refer to BaselineThe New Format and Content (Mar. Pollut. Bull. 42, 703704).</p><p>Dynamics of trace metal concentrations in an intertidal rockyshore food chain</p><p>Wen-Xiong Wang *, Pan Wong</p><p>Department of Biology, The Hong Kong University of Science and Technology (HKUST), Clear Water Bay, Kowloon, Hong Kong</p><p>Numerous studies have measured the concentrations ofvarious trace metals in marine organisms (for a review seeEisler, 1981; Ne, 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 arequantied. 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).</p><p>Trophic transfer has increasingly been recognized as animportant pathway for metal accumulation in marineinvertebrates (Wang and Fisher, 1999; Wang, 2002). Bio-</p><p>magnication occurs when the metals are transportedthrough a food chain at increasing concentrations in theanimals at higher trophic levels. Metal biomagnicationhas long been recognized as occurring with Hg (mainly inits methylated form, methylmercury) and cesium (Wang,2002). Evidence has largely come from measurements insh or other higher level organisms (e.g., birds, ducks).</p><p>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 biomagnication in such foodchains. Intertidal rocky shores host diverse species of inver-tebrates that dier tremendously in their metal accumula-tion patterns and thus metal concentrations, even amongthe closely related species such as bivalves (e.g., musselsand oysters).</p><p>In this study, the concentrations of ve 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 biomagnication 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 starsh, which</p><p>* Corresponding author. Tel.: +852 23587346; fax: +852 23581559.E-mail address: wwang@ust.hk (W.-X. Wang).</p><p>www.elsevier.com/locate/marpolbul</p><p>Marine Pollution Bulletin 52 (2006) 332356</p></li><li><p>was only occasionally observed in this area. Clear WaterBay is in the eastern part of Hong Kong and subjected tosignicant inuence from ocean currents. The bay can beconsidered relatively pristine, without signicant impactfrom anthropogenic activity. The salinity of the bay israther constant throughout the dierent seasons (typically2532 ppt).</p><p>The invertebrates were collected from an exposed shorein a rocky area. All species except the oyster S. cucullatawere collected from June 2003 to June 2004. The oysterswere collected from July 2003 to June 2004. For the barna-cles, ve bodies were combined into one sample, becausethe mass of an individual organism was too small for metalanalysis. For the other species, 68 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.</p><p>In the laboratory, the animals were dissected usingstainless steel knives and briey 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)(PerkinElmer, 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 certied values areshown in Table 1. Recoveries were 90110% 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.</p><p>Over the one-year sampling period, the tissue dryweights of the mussels and oysters were much lower duringAugustNovember 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 (JulySeptember) than duringthe other seasons, again probably caused by reproduction.</p><p>There was no clear pattern of tissue dry weight for thesnails through the seasons. It should be noted that only68 replicates were collected at each sampling time, andeorts were made to select comparable body sizes in eachmonthly sampling.</p><p>The metal concentrations were rst correlated with thetissue dry weight of the animals using an allometric powerfunction (Boyden, 1974, 1977). Signicant 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 signicant correlation wasfound for the barnacles or snails, presumably because thebody tissue weights were within a narrow range (0.160.4 g for each composite of ve individual barnacles, and0.100.21 g for snails) throughout the dierent seasons.Interestingly, the allometric coecients 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</p><p>Table 1Comparison of the certied metal concentrations in the oyster standardreference and the measured values (lg g1)</p><p>Certied values std Measured values std % Recovery</p><p>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</p><p>mussel</p><p>Tiss</p><p>ue d</p><p>ry w</p><p>eigh</p><p>t (g)</p><p>0.00</p><p>0.25</p><p>0.50</p><p>0.75</p><p>1.00</p><p>snail</p><p>06/20</p><p>0307</p><p>/2003</p><p>08/20</p><p>0309</p><p>/2003</p><p>10/20</p><p>0311</p><p>/2003</p><p>12/20</p><p>0301</p><p>/2004</p><p>02/20</p><p>0403</p><p>/2004</p><p>04/20</p><p>0405</p><p>/2004</p><p>06/20</p><p>04</p><p>0.0</p><p>0.1</p><p>0.2</p><p>0.3barnacle</p><p>06/20</p><p>0307</p><p>/2003</p><p>08/20</p><p>0309</p><p>/2003</p><p>10/20</p><p>0311</p><p>/2003</p><p>12/20</p><p>0301</p><p>/2004</p><p>02/20</p><p>0403</p><p>/2004</p><p>04/20</p><p>0405</p><p>/2004</p><p>06/20</p><p>04</p><p>0.0</p><p>0.2</p><p>0.4</p><p>0.6</p><p>oyster</p><p>0.0</p><p>0.2</p><p>0.4</p><p>0.6</p><p>0.8</p><p>Fig. 1. Seasonal variations in tissue dry weight of the collected inverte-brates. For barnacles, each measurement represents ve bodies. Mean SD (n = 68).</p><p>Table 2Size allometric coecients (b) of metal concentrations in the black musselSeptifer virgatus and the rock oyster Saccostrea cucullata</p><p>Septifer virgatus Saccostrea cucullata</p><p>b r2 b r2</p><p>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***</p><p>r2: Correlation coecient. No relationship was found for the barnaclesand snails. NS: not signicant.** Signicant at the p &lt; 0.01 level.*** Signicant at the p &lt; 0.001 level.</p><p>Baseline / Marine Pollution Bulletin 52 (2006) 332356 333</p></li><li><p>and Fisher, 1997). Very dierent power coecients havebeen found in these studies.</p><p>To avoid any inherent inuence 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 coecients (with signi-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 ve metals in S. virgatus, S. cucul-lata, T. japonica, and M. musiva. Generally, metal concen-trations varied signicantly through the seasons (one-wayANOVA, p &lt; 0.001 for all metals and species, except Znin snails (p &lt; 0.01), Cu in oysters (p &lt; 0.05), and Zn in bar-nacles (p &lt; 0.05)). The only exception was Cu in the snails,which was not signicantly inuenced by the season(p &gt; 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.</p><p>Ag concentrations in the black mussels were much lowerthan in the other three species, with typical concentrationsof 0.010.06 lg g1. Concentrations in the oysters (0.72.8 lg g1) were higher than those in the barnacles (0.61.4 lg g1). The predators contained the highest Agconcentrations (e.g., as high as 10 lg g1 during October</p><p>and December). Cd concentrations in the three prey specieswere rather comparable (1.55.0 lg g1), but were highestin the snails (e.g., 11.7 lg g1 in August). For Cu, oystersand snails contained the highest concentrations, both inthe range 300880 lg g1, whereas Cu concentrations werelowest in the barnacles. The concentrations of Se in themussels and oysters were comparable (1.63.8 lg g1),and its concentration in the snails was the highest (6.715 lg g1). Similar to Cu, the concentrations of Zn in theoysters and snails were the highest (6303080 lg g1), butthe barnacles also contained very high Zn concentrationsin their bodies (8201200 lg g1). The concentration ofZn in the mussels was the lowest among the four species(53108 lg g1).</p><p>The data show striking dierences in the metal bodyconcentrations in dierent species of marine invertebrates,even among the taxonomically close species. It is interest-ing to note the very low Ag concentrations in the blackmussels (0.010.06 lg g1). Such low values are in strongcontrast to Ag concentrations measured in the commonmussel Mytilus edulis collected from dierent regions ofUS coastal waters (geometric mean of 0.17lg g1, OCon-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 0.040.17lg g1, but much higher concentrationswere found in the coastal population (0.210.28lg g1).The lower Ag concentration was attributed to higher Ageux 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 dierences 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 (OConnor, 1992).</p><p>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 dicult 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 ve metals examined, thegreatest dierences in metal concentrations among dierentspecies were found for Cu and Zn, which varied by 50130times and 1532 times, respectively. The high Zn concen-trations in the barnacles and oysters were mainly causedby their very ecient dietary assimilation, as well as bythe exceedingly low rate of Zn eux from these animals(Wang et al., 1999; Ke and Wang, 2001). Wang et al.(1999) were able to predict the phenomenal Zn concentra-</p><p>0</p><p>5</p><p>10</p><p>15</p><p>20musselsoystersbarnaclessnails</p><p>Ag</p><p>06/20</p><p>0307</p><p>/2003</p><p>08/20</p><p>0309</p><p>/2003</p><p>10/20</p><p>0311</p><p>/2003</p><p>12/20</p><p>0301</p><p>/2004</p><p>02/20</p><p>0403</p><p>/2004</p><p>04/20</p><p>0405</p><p>/2004</p><p>06/20</p><p>04</p><p>0</p><p>5</p><p>10</p><p>15</p><p>20</p><p>06/20</p><p>0307</p><p>/2003</p><p>08/20</p><p>0309</p><p>/2003</p><p>10/20</p><p>0311</p><p>/2003</p><p>12/20</p><p>0301</p><p>/2004</p><p>02/20</p><p>0403</p><p>/2004</p><p>04/20</p><p>0405</p><p>/2004</p><p>06/20</p><p>04</p><p>10</p><p>100</p><p>1000</p><p>1</p><p>10</p><p>100</p><p>1000</p><p>0</p><p>4</p><p>8</p><p>12</p><p>16</p><p>Zn</p><p>Se</p><p>Cu</p><p>Cd</p><p>Met</p><p>al c</p><p>once</p><p>ntra</p><p>tion </p><p>in ti</p><p>ssue</p><p> (g g</p><p>)-1</p><p>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 = 68).</p><p>334 Baseline / Marine Pollution Bulletin 52 (2006) 332356</p></li><li><p>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 eux (Ke and Wang, 2001).In contrast to barnacles and oysters, the assimilation e-ciency of Zn in mussels is generally lower, and its euxmuch 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.</p><p>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 biomagni-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 (oys...</p></li></ul>