Bioaccumulation of Some Heavy Metals on Freshwater Crayfish

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1 Pollution Science, Technology and Abatement, Impact, Monitoring and Management of Environmental Pollution,2010: ISBN: Bioaccumulation of Some Heavy Metals on Freshwater Crayfish Utku GÜNER Trakya University, Department of Biology, Edirne Turkey Tel: Fax:

2 2 Utku Güner Abstract: Anthropogenic inputs of pollutants such as heavy metals into the marine environment have increased their levels to large extents within past few decades. The available literature on heavy metal bioaccumulation by freshwater crayfish has been analyzed. A very uneven data distribution was found, Orconectes, Cambarus Procambarus and Astacus are the most commonly investigated orders of crayfish. Furthermore, Zn, Cu, Pb and Cd are the most intensively researched heavy metals, and only infrequent investigations of other metals are documented. At some conditions bioaccumulation levels of some heavy metals were as follows Mn> Zn >Cu>Ni>Cr>Pb>Cd. Accumulated metal concentrations are interpreted in terms of different trace metal accumulation patterns, dividing accumulated metals into two components metabolically available metal and stored detoxified metal. The following chapter will focus on bioaccumulation of some heavy metals on freshwater crayfish. Correspondence/ Reprint request: Dr. Utku Güner, Department of Biology, Trakya University, Edirne Turkey uguner@trakya.edu.tr INTRODUCTION Freshwater crayfish, the largest and the most valuable invertebrate of all inland waters, feed on detrius zoobentic animals and aquatic plants. Being amnivorus, freshwater crayfish play an important role in the trophic chain of benthic communities in all inland waters (lakes, rivers etc.) and contribute in regulation of freshwater ecosystems. Freshwater crayfish species such as Astacus, Orconectes and Cambarus are considered as biological indicators of clean waters because of their relatively lower locomotory activity in comparison with fresh water fish. In general, the term Heavy Metal is used by the environmentalists and biologists where there are connotations of toxicity. Solubility of heavy metals in freshwater is controlled by factors such as ph, salinity, temperature and presence of different anions. A number of highly sensitive analytical techniques are available for accurate and reliable measurements of toxic heavy metals in freshwaters, lakes, river sediments and freshwater biota. Some heavy metals (except Cd, Pb and Hg) have important biological roles at low concentrations but show toxic effects at higher concentrations (Zn, Cu). Toxicity of heavy metals depends upon the metal concentration and speciation and hysiology of the target freshwater crayfish species (Fig1). A number of metals are toxic because of their strong interaction with sulphur containing biochemicals. Heavy metals may

3 Heavy metals on Crayfish 3 be accumulated by crayfish from the polluted water body and river, lake sediments. Heavy metals are natural constituents of freshwater environment, generally found in very low concentrations. Human activity has inevitably increased the levels of metal ions in many of these natural water systems. Mine drainage, river oil and gas exploration, industrial (pesticides, paints, leather, textile, fertilizers and pharmaceuticals) and domestic effluents, agricultural runoff, acid rain etc. have all contributed to the increased metal load in these waters being ultimately incorporated into aquatic sediments. The behavior of metals in natural waters is a function of the substrate sediment composition, the suspended sediment composition and the water chemistry. Sediment composed of fine sand and silt will generally have higher levels of adsorbed metal than quartz, feldspar, and detrital carbonate-rich sediment. Metals also have a high affinity for humic acids, organo-clays and oxides coated with organic matter [1-2]. The water chemistry of the system controls the rate of adsorption and desorbtion of metals to and from sediment. Adsorption removes the metal from the water column and stores the metal in the substrate. Desorption returns the metal to the water column, where recirculation and bioassimilation may take place. Metals may be desorbed from the sediment if the water experiences increases in salinity, decreases in redox potential, or decreases in ph. Salinity increase: Elevated salt concentrations create increased competition between actions and metals for binding sites. Often, metals will be driven off into the overlying water. (Estuaries are prone to this phenomenon because of fluctuating river flow inputs.) Redox Potential decrease: A decreased redox potential, as is often seen under oxygen deficient conditions, will change the composition of metal complexes and release the metal ions into the overlying water. ph decrease: A lower ph increases the competition between metal and hydrogen ions for binding sites. A decrease in ph may also dissolve metal-carbonate complexes, releasing free metal ions into the water column [1-2] Heavy metals in surface water systems can be from natural or anthropogenic sources. Currently, anthropogenic inputs of metals exceed

4 4 Utku Güner natural inputs. Excess metal levels in surface water may pose a health risk to humans and to the environment Figure 1. Target tissue of heavy metals on freshwater crayfish. According to the toxicity to adult crayfish determined during an acute toxicity test heavy metals can be divided into several categories [3]; Table 1). Copper, upon the mentioned classification falls into the 5 th category of toxicity, i.e. in the scale of toxicity to crayfish copper is closer to non-toxic elements and their compounds. Table 1. Ranking of the 96-h values for adult crayfish [3]. Rank LC 50 range, µg/l Relative toxicity Extremely toxic > Nearly non-toxic Heavy metals like Cu, Zn and Fe are essential for fish metabolism while some others such as Mo, Ag, Cr, Pb, Ni and Cd have no known role in biological systems (Fig 2).

5 Heavy metals on Crayfish 5 Heavy metals essential for crayfish metabolism no known role in biological systems Cu Zn Mo Cr Ni Ag Pb Cd Figure 2. Type of metals for freshwater crayfish. Any aquatic invertebrate will take up trace metals into the body from solution through permeable body surfaces and from the gut. Recently it has become increasingly appreciated that uptake of trace metals from the diet may be the major source of metals for many aquatic invertebrates [4], including barnacles [5-6] Fig. 1 presents a schematic representation of the accumulation of a trace metal by a decapod crustacean [7]. Metal passively adsorbed onto the exoskeleton of a crustacean (with the potential to be desorbed when dissolved conditions change) will contribute to the total body concentration of metal in the crustacean, but its proportional contribution is usually small [7-10]. Since, furthermore, such metal does not enter physiological pathways within the animal, it is not considered further here. When metal first enters the body of the crustacean after uptake either from solution through permeable ectodermal surfaces or across the endoderm of the gut, it will initially be metabolically available that is it has the potential to bind to molecules in the receiving cell or elsewhere in the body after internal transport via the haemolymph (Fig. 1). In the case of an essential metal, it is available to bind to sites where it can play an essential role (e.g. zinc in the enzyme carbonic anhydrase or copper in haemocyanin) or, if present in excess (caused by entry at too high a rate), to sites where it may cause toxic effects. Such an excess of essential metal (and all non-essential metal) must be detoxified, i.e. bound tightly to a sacrificial site from which escape is limited, probably in a storage organ beyond the site of uptake. The metal has now entered the second component of accumulated metal the detoxified store (Fig. 3) which may be temporary or permanent. Trace metals taken up into the body may or may not be excreted, either from the metabolically available component or from a detoxified store (Fig. 3), dependent on the accumulation pattern.

6 6 Utku Güner Figure 3. A schematic representation of the body metal content of Crayfish. In general the highest metal content of heavy metals were detected in the hepatopancreas, which is prime site for metal storage and detoxification. On the other hand the lowest heavy metals content was found in abdominal muscles. Some heavy metals like Ni and Cr present in carapace (exoskeleton) because this tissue was involved in absorption and excretion of these metals. The concentrations at which metals may be considered important vary as some are essential at low levels yet toxic at others. Criteria for establishing whether or not a trace heavy metal is essential for the normal healthy growth of plants and /or animals include: The organism can neither grow nor complete its life cycle without an adequate supply of the element; The element cannot be wholly replaced by any other element; The element has a direct influence on the organism and is involved in its metabolism [11].

7 Heavy metals on Crayfish 7 Table 2. Criteria used to evaluate the risks of Pb, Zn, and Cd in fish and crayfish to humans and wildlife. Criterion a Units Pb Cd Zn Source TDI/PTDI lg/kg body wt/day 3.57 b 1.0 nv WHO PTWI lg/kg body wt/week 500c nv WHO PTDI lg/day 6 d nv nv USFDA MRL lg/kg body wt/day nv 0.2 nv ATSDR ML (fish) lg g 1 wet-wt nv FAO/WHO ML (crustaceans) lg g 1 wet-wt nv FAO/WHO RfD lg/kg body wt/day nv USEPA SV (recreational fishers) lg g 1 wet-wt nv 4.0 nv USEPA SV (subsistence fishers) lg g 1 wet-wt nv nv USEPA RDA l g/kg body wt/day nv nv 160 ATSDR NOAEL-TRV (avian) mg/kg body wt/day e USEPA NOAEL-TRV (mammal) mg/kg body wt/day e USEPA a TDI, tolerable daily Intake; PTDI, provisionally tolerable daily intake; PTWI, provisionally tolerable weekly intake; MRL, minimum risk level; ML, maximum allowable concentration; RfD, reference dose; SV, screening value; RDA, recommended daily allowance; NOAEL, no observed adverse effect level; TRV, toxicity reference value;nv, no value; b For children and adults ; c For adults; no value for children; d For children; no value for adults; e Interim value; consensus value pending WHO, World Health Organization; USFDA, US Food and Drug Administration; FAO, Food and Agricultural Organization of the United Nations; ATSDR, (US) Agency for Toxic Substances and Disease Registry; USEPA, US Environmental ProtectionAgency; Many heavy metals are detoxified in the form of one of a variety of insoluble granules or deposits in invertebrate tissues ([12-13] There are three types of intracellular granules were described: type A consisting of concentric layers of calcium and magnesium phosphates which may contain trace metals such as manganese and zinc; type B more heterogeneous in shape and always containing sulphur in association with metals that include copper and zinc;

8 8 Utku Güner type C often polyhedral with a crystalline form, mainly containing iron, probably derived from ferritin. Figure 4. Model for coupled MT induction and rescue of target ligands comprised by inappropriate metal binding, by Cd in this example. (MT, metallothionein; MRE, metal regulatory element; MTF, metal transcription factor; MTI, metal transcription inhibitor [14]. In crustaceans, the most commonly reported metal-rich granules are type A and B granules [15-17] while large ferritin crystals are haracteristic of the ventral caecum cells of stegocephalid amphipods [18]. Detoxification also occurs in the soluble phase. Certain trace metals (e.g. Zn, Cu, Cd, Ag, Hg) are associated with, and induce, metallothioneins, low molecular weight cytosolic proteins involved in the cellular regulation and detoxification of these metals [14-19].The presence of sulphur in the high proportion of cysteine residues in these proteins provides the high metal affinity of the molecule, sequesteringmetals in the cytoplasmand reducing their metabolic availability. It is the lysosomal breakdown of Metallothioneins that probably gives rise to the sulphur-rich type B granules described above, as in the amphipod Orchestia gammarellus.

9 Heavy metals on Crayfish 9 1. ESSENTIAL METALS 1.1 Copper Organic wastes of industrial and agricultural origin enter aquatic ecosystems and Cu may exist in ionic form or be complexed to organic and inorganic ligands. Cu pollution throughout the world is increasing due to mining and industrial activities and environmental contamination by Cu occurs from weathering of minerals, rocks and anthropogenic sources. Table 3. Essential metal requirements in enzymes of metabolising soft tissue [8]. Copper Zinc Number of metal-associated enzymes Percentage of total number of enzymes 1.40% 3.74% Average number of metal atomsper enzyme molecule Estimated enzyme metal requirement in tissue (µg g 1 dry wt) Copper (Cu) is plentiful in the environment and essential for the normal growth and metabolism of all aquatic organisms [20-21]. Abnormal levels of copper intake may range from levels so low as to induce a nutritional deficiency to levels so high as to be acutely toxic. Crayfish (Cambarus bartoni) were accumulated copper concentrations ranging from 130 to 296 mg/kg after exposure to copper concentrations ranging from 125 to 500 µg/litre for 4 weeks. Copper was predominantly accumulated in the gills and hepatopancreas [21]. Exposure of crayfish (Cambarus bartoni) to 12.5 mg Cd/l for 72 h results in significantly increased copper stores in the hepatopancreas; however, isopods similarly exposed had decreased copper stores in antennal glands [22]. In the rusty crayfish (Orconectes rusticus), toxicity of copper at high concentrations is due to the coagulatory action on cellular proteins and to interference with respiratory processes; at low concentrations, copper causes degenerative changes in certain tissues and interferes with glutathione equilibrium [23]. Larvae of the red crayfish (Procambarus clarkii) exposed to copper as embryos are less sensitive than those exposed after hatching, suggesting acclimatization [24].

10 10 Utku Güner Table 4. Crayfish, Cambarus bartoni; copper-tolerant strain exposed to 19 (controls), 125, 250, or 500 mg/l for 4 weeks; concentrations in controls (mg/kg DW) vs. all experimental groups (mg/kg DW). Tissue Bioaccumulation Exoskeleton 54 DW vs DW Gills 368 DW vs. 5711,167 DW Hepatopancreas 1,778 DW vs. 1,4942,346 DW Muscle 88 DW vs DW Viscera 92 DW vs DW 1.2 Zinc Zinc (Zn) is an essential trace element for all living organisms. As a constituent of more than 200 metalloenzymes and other metabolic compounds, zinc assures stability of biological molecules such as DNA and of biological structures such as membranes and ribosomes [25]. Crustaceans can regulate body concentration of zinc against fluctuations in intake, although the ways in which regulation is achieved vary among species [21]. Regulation of whole body zinc to a constant level is reported for many crustaceans, including intertidal prawns (Palaemon spp.), sublittoral prawns (Pandalus montagui), green crabs (Carcinus maenus), lobsters (Homarus gammarus), amphipods (Gammarus duebeni), isopods (Asellus communis), and crayfish (Austropotamobius pallipes; [7-10, 27]. The body zinc concentration at which zinc is regulated in crustaceans usually increases with increasing temperature, salinity, molting frequency, bioavailability of the uncomplexed free metal ions, and chelators in the medium [9-10, 28-29]. Freshwater crayfish (Orconectes virilis) are among the more resistant crustaceans (LC 50 value of 84 mg Zn/l in 2 weeks) and can easily tolerate the recommended water quality criteria of µg/l; nevertheless, some streams in Arkansas and Colorado contain mg Zn/l [30]. Orconectes virilis exposed to extremely high sublethal ambient zinc concentrations of 63 mg/l for 2 weeks show whole body BCF values of only 2; a similar pattern was observed at other concentrations. In all cases, zinc tended to concentrate in gills and hepatopancreas at the expense of muscle, carapace, and intestine [30]. In freshwater crayfish

11 Heavy metals on Crayfish 11 (Procambarus acutus acutus), the major uptake route was the ambient medium and not diet, although retention time of dietary zinc was greater [31]. When dietary zinc was the only zinc source, crayfish rapidly reached a steady state; when water was the only zinc source, crayfish did not reach a steady state [31]. Zinc concentrations in the freshwater crayfish Austropotamobius pallipes pallipes normally range from about 1 µg./g. in the blood to 100 µg./g. in the hepatopancreas. The permeability of the body surface to zinc is very low. Long exposure to concentrations exceeding that of the blood is required to increase the internal tissue zinc concentrations appreciably. Much of the zinc which is absorbed from solution appears to be adsorbed on to the gill and shell surfaces. Most of the body zinc is obtained from food. The hepatopancreas is the principal organ of zinc regulation. It can absorb excess zinc from the stomach fluid and can remove excess zinc if this is injected into the blood. Very little of the excess zinc in the hepatopancreas can be lost in the urine or across the body surface. Zinc is lost only when the animal feeds and faeces are produced to which it can bind. As the amount of zinc in the food increases, a smaller percentage of it is absorbed by the hepatopancreas and more is lost in the faeces. Regulation of zinc seems to depend on changes in the hepatopancreas/stomachfluid ratio. These alter the availability of zinc for removal in the faeces according to the concentration in the hepatopancreas. There is no close relationship between the behaviour of zinc and copper although zinc is bound to blood proteins some of which are haemocyanins. Differences in the methods of regulation between the freshwater crayfish and the marine lobster may represent changes which have occurred during the penetration of the crayfish into fresh water [32]. Table 5. Dose and effect of zinc for crayfish and crab. Animals Dose Effect Crayfish, Orcenectes virilis 130,000 No deaths in 10 days Hermit crab, Pagurus longicarpus Adult 200 LC 50 (168 h) Adult 400 LC 50 (96 h)

12 12 Utku Güner 2. NON ESSENTIAL METALS 2.1 Cadmium Non-ferrous metal mines represent a major source of cadmium released to aquatic environment. Cd is a non-essential, extremely toxic trace element [33] and typically found at low (i.e. parts per billion) concentrations in rivers, lakes and ponds. There is no evidence that Cd is biologically essential or beneficial; on the contrary, it has been implicated as the cause of numerous human deaths and various deleterious effects in fish and wildlife. In sufficient concentration, it is toxic to all forms of life, including microorganisms, aquatic animals, and crayfish [34]. Decapod crustaceans are the most sensitive marine group in short-term tests; LC 50 (96 h) values ranged from 320 to 420 ppb for the grass shrimp (Palaemonetes vulgaris), the hermit crab (Pagurus longicarpus), and the sand shrimp (Crangon crangon) [35]. Studies of longer duration demonstrated that survival of shrimp groups was low at >250 ppb during 6 weeks of exposure and that hermit crab deaths were recorded at 60 ppb after 6 weeks, although some survivors remained at 10 weeks when the studies ended [36]. In another study, an LC 50 range of 14.8 to 19.5 ppb Cd was reported for two species of mysid shrimp subjected to lifetime (i.e., 23 to 27 days) exposure to cadmium salts [34]. Table 6. Bioconcentration of Cadmium for Homarus americanus and Pontoporeia affinis. Crayfish Ambient Exposure period Bioconcentration period, concentration ppb week factor, whole organism Homarus americanus Pontoporeia affinis Silver Silver (Ag) is toxic to aquatic organisms when present as ionic silver (Ag + ). In freshwater fish, toxicity occurs because silver specifically inhibits the activity of sodium/potassiumadenosine triphosphatase (Na/K-ATPase), thereby blocking Na + and Cl 2 uptake and causing death from ionoregulatory failure However, natural ligands such as Cl 2 and dissolved organic matter greatly reduce the toxicity of silver by the formation of silver complexes [37]. The Freshwater crayfish (Cambarus diogenes diogenes) exhibits silver uptake and accumulation patterns similar to that of the few freshwater teleost fish in which the physiology of silver toxicity has been investigated. In addition, it appears that the main toxic action of silver in this freshwater crustacean is similar to that reported for teleost fish. One clear exception,

13 Heavy metals on Crayfish 13 however, is the elevated Na + efflux observed during the first 24 h of silver exposure. Based on the similarities between silver-induced physiological disturbances in freshwater crayfish and teleost fish, it appears that much of the current understanding of silver toxicity and how it is modulated by environmental factors (arising from studies on fish) may apply also to invertebrate [37]. 2.3 Nickel Nickel (Ni) is ubiquitous in the biosphere. Nickel introduced into the environment from natural or human sources is circulated through the system by chemical and physical processes and through biological transport mechanisms of aquatic organisms [38]. Nickel concentrations are comparatively elevated in aquatic plants and animals in the vicinity of nickel smelters, nickel-cadmium battery plants, electroplating plants, sewage outfalls, coal ash disposal basins, and heavily populated areas [1, 39-45] For example, at Sudbury, Ontario, mean nickel concentrations, in mg/kg DW, were 22 for larvae of aquatic insects, 25 for zooplankton, and 290 for aquatic weeds; maximum concentrations reported were 921 mg/kg DW in gut of crayfish (Cambarus bartoni) and 52 mg/kg fresh weight (FW) in various fish tissues [44-45]. For all aquatic species collected, nickel concentrations were highly variable between and within species; this variability is attributable, in part, to differential tissue uptake and retention of nickel, depth of collection, age of organism, and metal-tolerant strains [1,26, 44-47]. In aquatic ecosystems, nickel was accumulated from the water column by periphyton, rooted aquatic macrophytes, zooplankton, crayfish, clams, and fishes. However, there was no evidence of food chain biomagnification of nickel in the Sudbury ecosystem [48]. For example, in the nickel-contaminated Wanapitei River, bioconcentration factors during summer 1974 were highest for whole periphyton (19,667), followed by whole pondweeds (11,429), sediments (5,333), whole crayfish (929), whole zooplankton (643), muscle of carnivorous fishes (329), soft tissues of clams (262), and muscle of omnivorous fishes (226) [48]. 2.4 Mercury The element mercury (Hg) and its compounds have no known normal metabolic function. Their presence in the cells of living organisms represents contamination from natural and anthropogenic sources; all such contamination must be regarded as undesirable and potentially hazardous [49]. Elimination of accumulated mercury, both organic and inorganic, from aquatic organisms is a complex multicompartmental process, but appears to be

14 14 Utku Güner largely dependent on its rate of biological assimilation. This rate, in turn, varies widely (20% to 90%) between species, for reasons as yet unexplained [49]. For example, mercury associated with dietary components that are not assimilated is eliminated rapidly with feces. The rest is absorbed across the gut and incorporated into tissues. This assimilated fraction of mercury is depurated much more slowly, at a rate positively correlated with the organism's metabolism [49-50]Time to eliminate 50% of biologically assimilated mercury and its compounds (Tb 1/2) is variable. Among various species of freshwater teleosts, Tb 1/2 values (in days) were 20 for guppies Poecilia reticulatus, 23 for goldfish Carassius auratus, 100 for northern pike, and 1,000 each for mosquitofish Gambusia affinis, brook trout, and rainbow trout [51] ( similar range in. Tb 1/2 values was recorded for invertebrates and marine fishes: 297 days for the crayfish Astacus fluviatilis, 435 days for mussel, 481 days for the clam Tapes decussatus 1,030 days for the eel Anguilla vulgaris, and 1,200 days for the flounder Pleuronectes flesus [49]. 2.5 Lead Lead (Pb) has been known for centuries to be a cumulative metabolic poison; however, acute exposure is lessening. Of greater concern is the possibility that continuous exposure to low concentrations of the metal as a result of widespread environmental contamination may result in adverse health effects [49-51] Environmental pollution from Pb is now so high that body burdens in the general human population are closer than the burdens of any other toxic chemical to those that produce clinical poisoning [52]. Further, Pb is a mutagen and teratogen when absorbed in excessive amounts, has carcinogenic or cocarcinogenic properties, impairs reproduction and liver and thyroid functions, and interferes with resistance to infectious diseases [53]. Sediments are not only sinks for Pb but may act as a source of Pb to aquatic biota after contamination from the original source has subsided [54]. The uptake of Pb from artificially contaminated pond sediments was recorded in roots and foliage of submersed aquatic macrophytes (Potamogeton foliosus, Najus guadalupensis) and in the exoskeleton of crayfish (Orconectes nais). Accumulation of Pb in crayfish primarily was through adsorption; most was lost through molting, though some internal uptake and elimination occurred without molting [54]. Crustacean molts represent 15% of the Pb body burden and are probably more significant than fecal pellets in Pb cycling processes [55]. 2.6 Molybdenum Molybdenum (Mo) is present in all plant, human, and animal tissues, and is considered an essential micronutrient for most life forms [ ].

15 Heavy metals on Crayfish 15 The first indication of an essential role for Mo in animal nutrition came in 1953 when it was discovered that a flavoprotein enzyme, xanthine oxidase, was dependent on Mo for its activity [56]. It was later determined that Mo is essential in the diet of lambs, chicks, and turkey poults [56]. Molybdenum compounds are now routinely added to soils, plants, and waters to achieve various enrichment or balance effects [57-58]. Limited data suggested that aquatic invertebrates were very resistant to Mo; adverse effects were observed on survival at >60 mg Mo/l and on growth at >1,000 mg Mo/l Bioconcentration factors were low, but depending on initial dose, measured residues (mg/kg fresh weight) were as high as 16 in amphipods, and were 3 in clams, 18 in crayfish muscle, and 32 in crayfish carapace [59-61]. Acknowledgements I thank Dr. Volkan AKSOY for his careful reading of, and helpful comments on, an earlier version of this manuscript. REFERENCES 1. Eisler, R. (1981). Trace metal concentrations in marine organisms. Pergamon Press, New York. 687 pp. 2. Eisler, R. (1984). Trace metal changes associated with age of marine vertebrates. Biol. Trace Element Res. 6: Eversole, A. G. (1980). Effects of water-borne mirex on the survival and production of Macrobrachium rosenbergii (de Man). Water Resour. Res. Inst., Clemson Univ., Clemson SC, OWRT Proj. B-115-SC. 44 pp. 4. Wang, W-X. (2002). Interactions of trace metals and different marine food chains. Mar Ecol Prog Ser, 243, Wang W-X. Qiu J-V. Qian P-I, (1999a). Significance of Trophic Transfer in Predicting the High Concentration of Zinc in Barnacles. Environ. Sc.i Technol., 33, Wang W-X. Qiu J-V. Qian P-I, (1999b). The trophic transfer of Cd, Cr. and Se in the barnacle Balanus amphitrite from planktonic food Mar Ecol Prog Ser, Rainbow, R S., and S. L White. (1989). Comparative strategies of heavy metal accumulation by crustaceans: zinc, copper and cadmium in a decapod, an amphipod and a barnacle. Hydrobiologia 174:245-26

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