Polar Biol (1997) 17: 131—140 ( Springer-Verlag 1997

ORIGINAL PAPER

J.E.A. de Moreno · M.S. Gerpe · V.J. MorenoC. Vodopivez

Heavy metals in Antarctic organisms

Received: 17 July 1995/Accepted: 11 April 1996

Abstract To evaluate levels of essential (zinc and cop-per) and non-essential (mercury and cadmium) heavymetals, 34 species of organisms from different areasclose to the Antarctic Peninsula were analysed. Theseincluded algae, filter-feeders, omnivorous invertebratesand vertebrates. Mercury was not detected, while cad-mium was found in the majority of organisms analysed(detection limit was 0.05 ppm for both metals). Thehighest cadmium concentration was observed in thestarfish Odontaster validus. Anthozoans, sipunculidsand nudibranchs showed maximum levels of zinc, whilethe highest copper level was found in the gastropod¹rophon brevispira. Mercury and cadmium levels infishes were below the detection limit. Concentrations ofessential and non-essential metals in birds were highestin liver followed by muscle and eggs. Cadmium andmercury levels in muscle of southern elephant sealswere above the detection limit, whereas in Antarctic furseals they were below it. The objective of the study wasto gather baseline information for metals in AntarcticOcean biota that may be needed to detect, measure andmonitor future environmental changes.

Introduction

Antarctica is one of the most pristine areas of the world.However, in addition to isolated incidents such as ship-

J.E.A. de Moreno ( ) · V.J. MorenoDepartamento de Ciencias Marinas,Facultad de Ciencias Exactas y Naturales,Universidad Nacional de Mar del Plata,Funes 3350, 7600 Mar del Plata, Argentina

M.S. GerpeConsejo Nacional de Investigaciones Cientificas y Tecnicas(CONICET)

C. VodopivezInstituto Antartico Argentino, Cerrito 1248,1010 Buenos Aires, Argentina

wrecks (i.e. Bahıa Paraıso near Palmer Station in 1989and Nella Dan at the MacQuarie Islands in 1989),a continuous but low level of contamination does existdue to human settlements and their associated activ-ities, such as shipping, boating, and loading and un-loading of fuel and goods, etc. It is imperative that theenvironmental impact of these activities and the effectson organisms be monitored in order that a harmoniousand viable ecosystem can be developed and main-tained.

Marine organisms take up and accumulate tracemetals in soft tissues to concentrations several orders ofmagnitude above the environmental levels. In Antarc-tica, the anthropogenic pollution by heavy metals isnegligible and, also, the food webs are relatively simple,and therefore the bioaccumulation and biomagnifica-tion processes are supposed to be of lower magnitude.

Some data have been published on heavy metallevels in seawater (Honda et al. 1987; Nolting et al.1991), ice (Boutron et al. 1984), soil (Alam and Sadiq1993) and organisms such as crustaceans (Petri andZauke 1993; Yamamoto et al. 1987), but bioaccumula-tion of heavy metals in Antarctic food chains has beenstudied to a smaller degree (Honda et al. 1987).

This project was initiated to establish levels of essen-tial (zinc and copper) and non-essential (mercury andcadmium) trace metals in a wide range of organisms,including algae, invertebrates and vertebrates.

The organisms analysed were collected from differentsampling zones in the islands close to the Antarcticpeninsula and some samples were also taken a few daysafter the Bahıa Paraıo wreck in Arthur Harbour andBiscoe Bay (Anvers Island).

Materials and methods

The samples analysed were collected by Argentine scientists in theSouth Orkney, South Shetland and Anvers Islands (Fig. 1), duringthree summer seasons from 1987 to 1989. Arthur Harbour and

Fig. 1 Sampling stations in the Antarctic Ocean: 1 Artigas Base62°13@S 58°56@W (King George Is.); 2 Pratt Base 62°30@S 59°41@W(Greenwich Is.); 3 Copper Mine 62°23@S 59°42@W (Robert Is.);4 Ferras Base 62°05@S 60°49@W (King George Is.); 5 Jubany Base62°14@S 58°38@W (King George Is.); 6 Laurie Is 60°46@S 44°42@W(@South Orkney Is.); 7 Arthur Harbour 64°46@S 64°06@W (Anvers Is.);8 Biscoe Bay 64°47@S 64°02@W (Anvers Is.)

Table 1 Species studied in the Antarctic Ocean and Stations sam-pled (see Fig. 1) (ND not determined)

Organisms studied Stations

Algae, Phaeophyta Durvillea antarctica 1Adenocystis sp. 1Ascoseira sp. 1Cytosphaera sp. 5Desmarestia sp. 5, 7Rodophyta Iridaea sp. 1¸eptosomia simplex 1, 8Chlorophyta ND 7, 8Porifera 1Anthozoa 1Nemertinea Parborlasia corrugatus 1, 2Sipuncula 1Polychaeta 2, 7Brachiopoda 7Bryozoa 3Gastropoda Nacella concinna 1, 5, 7, 8¹rophon brevispira 1Nudibranchia 2Amphipoda ¼aldeckia obesa 3Isopoda Glyptonotus antarcticus 3Asteroidea Odontaster validus 1, 7Neomilaster georgianus 1, 3, 7Echinoidea Sterechinus neumayerii 1, 3Ophiuroidea Ophiacantha antarctica 4Ascidiacea Distaplia cylindrica 1, 2Fish Notothenia coriceps (notothenid) 6Birds Pygoscelis papua (gentoo penguin) 1P. adeliae (Adelie penguin) 1Phalacrocorax atriceps (blue-eyed shags) 1¸arus dominicanus (kelp gull) 5Sterna vitatta (Antarctic tern) 5Chionis alba (greater sheatbill) 1Mammals Arctocephalus gazella (Antarctic fur seal) 6Mirounga leonina (southern elephant seal) 1

Biscoe Bay samples were taken by a multidisciplinary team of theNational Science Foundation of the United States (Division of PolarPrograms) after the Bahıa Paraıso spill during the 1988/1989summer.

The species analysed and the sampling sites of the Antarcticmarine organisms are given in Table 1. All specimens were frozenbelow!20°C until treatment. Algae samples were dried to constantweight at 65°C and homogenized. Wet tissues were used for thedetermination of metal concentrations in the other organisms. In theeggs, the analyses were performed on the contents after removal ofthe shells.

Total mercury was determined using flameless atomic absorp-tion spectrophotometry, after wet mineralization of samples withnitric and sulphuric acids (1 : 4) and followed by potassium per-manganate digestion. Excess permanganate was reduced with hy-drogen peroxide solution (30%), and ionic mercury reduced to Hg0with tin (II) chloride (10%). The method was described by Morenoet al. (1984).

Concentrations of cadmium, copper and zinc were determined byatomic absorption spectrophotometry with an air-acetylene flame,and with a deuterium lamp for the background correction. Thesamples were digested with perchloric and nitric acids (1 :3) accordingto the methods previously reported by FAO/SIDA (1983). Analyticalreagents were used for the corresponding blanks and calibrationcurves. In order to assure quality control a certified reference material(mussel standard) provided by the National Institute for Environ-mental Studies (NIES, Tsukuba, Japan) was utilized. Determinationswere made with a Shimadzu AA-640-13 spectrophotometer. Thedetection limit of the method, for both Hg and Cd, was 0.05 ppm.

The differences between stations and metal levels differences be-tween sexes in Notothenia coriceps were both tested applying classi-cal ANOVA (assuming equality variances) using BMDP StatisticalSoftware, Inc. 12121 Wilshire Boulevard Suite 300 Los Angeles, CA90025 (1994). The relations between weight and heavy metal levelswere tested by regression analyses.

Results

Algae and invertebrates

In all the samples analysed, the levels of biologicallyactive or essential elements, i.e. zinc and copper, werepresent in the majority of the organisms at higher levelsthan the non-essential elements, like mercury and cad-mium. Levels of mercury were below the detection limitof the method (0.05 ppm). In contrast, cadmium wasdetectable in all the species analysed.

Metal concentrations detected in algae are listed inTable 2. The concentration range of each metal variedas follows: Cd"0.06—1.82 ppm, Zn"2.3—24.6 ppmand Cu"0.21—3.93 ppm in dry weight. Phaeophyta(Desmarestia sp., Cytosphaera sp. and Adenocystis sp.)and Chlorophyta showed high levels of Cd and, also,the first two accumulated high levels of Zn and Cu. Itshould be noted that the Cd concentrations of Adeno-cystis sp. were higher than those of Cu. Moreover, itsZn level was the lowest of all the algae studied. Consid-ering all the metals analysed, algae from Jubany andBiscoe Bay presented the highest values.

Cadmium, copper and zinc concentrations in filter-feeding invertebrates are shown in Table 3. Also thehigh levels of Zn in Polychaeta and Ascidiacea, and Cdin Porifera and Brachiopoda are noteworthy.

The metal concentrations in invertebrates with otherfeeding habits are shown in Table 4. This list includesstrict carnivores, such as the giant isopod Glyptonotus

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Table 2 Heavy metalconcentrations [mean (SD)/range, lg/g dry wt] in Antarcticalgae (ND not determined)

Species St (n) Cadmium Zinc Copper

Desmarestia sp. 7 (4) 0.36 (0.09) 16.48 (1.24) 1.19 (0.46)0.27—0.41 14.72—17.45 0.76—1.80

5 (2) 0.40 24.60 3.930.20—0.68 18.90—27.31 2.81—4.32

Durvillea antarctica 1 (3) 0.08 (0.03) 8.10 (0.20) 0.41 (0.35)0.06—0.12 7.90—8.30 0.11—0.80

Adenocystis sp. 1 (3) 0.48 (0.17) 2.30 (0.20) 0.21 (0.18)0.28—0.60 2.12—2.51 0.10—0.42

Ascoseyra sp. 1 (3) 0.07 (0.03) 8.21 (1.73) 0.51 (0.18)0.05—0.10 6.22—9.31 0.42—0.72

5 (2) 0.13 17.20 3.100.10—0.16 15.80—18.60 2.00—4.20

Cytosphaera sp. 5 (2) 1.10 17.20 3.450.90—1.20 16.80—17.60 3.00—3.90

Iridaea sp. 1 (3) 0.06 (0.01) 5.50 (0.48) 0.91 (0.03)0.05—0.08 5.01—5.99 0.53—1.32

¸eptosomia simplex 8 (4) 0.18 (0.04) 9.22 (0.55) 1.82 (0.17)0.13—0.22 7.23—11.43 1.68—2.06

1 (3) 0.08 (0.01) 6.67 (2.20) 0.91 (0.10)4.20—8.42 0.82—1.01

Chlorophyta ND 7 (8) 0.77 (0.13) 6.94 (2.48) 1.52 (0.31)0.59—0.94 4.55—12.14 1.00—1.98

8 (2) 1.82 9.61 2.301.63—2.01 7.19—12.03 2.17—2.43

Table 3 Heavy metalconcentrations [mean (SD)/range, lg/g wet wt] in Antarcticfilter-feeding invertebrates

Group St(n) Cadmium Zinc Copper

Porifera 1 (3) 3.71 37.37 3.153.48—3.84 25.08—45.85 2.72—3.46

Brachiopoda 7 (2) 4.33 26.70 4.873.70—4.95 25.56—27.82 4.66—5.07

Bryozoa 3 (1) 0.60 18.60 4.20

Distaplia cylindrica 1 (4) 0.49 52.82 0.300.01—1.01 44.74—58.56 0.29—0.30

2 (2) 0.28 42.12 0.330.26—0.30 40.00—44.20 0.14—0.52

Polychaeta 2 (2) 0.20 51.60 3.100.19—0.21 49.36—53.88 1.81—2.48

7 (2) 0.14 39.20 1.200.12—0.17 34.01—44.28 1.04—1.34

antarcticus and the gastropod ¹rophon brevispira, thelatter with a high copper level, and the grazer limpet(Nacella concinna) with high zinc and cadmium concen-trations in the middle intestinal gland. The other or-ganisms are omnivorous opportunistic invertebrates.Among them, the starfish (Odontaster validus) is out-standing, because of its high cadmium concentrations.Actinians, sipunculids and nudibranchs showed themaximum levels of zinc, followed by the gonads of seaurchins and nemerteans.

There were observed differences between some or-ganisms and heavy metals in different stations, but onlysome of them were significant. In algae, differences for

Zn, Cu and Cd were presented. The P-values corres-ponding to analyses of variance were 9.51]10~7 forZn, 9.20]10~3 for Cu and 0.0088 for Cd. Moreover,Zn showed significant differences between filter-feeders,and Cu between omnivorous species: the correspond-ing P-values for the ANOVA were 0.0343 and 0.0004,respectively.

Vertebrates

Levels of Hg were detected in most tissues of fishes,birds and mammals. Like algae and invertebrates, in

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Table 4 Heavy metal concentrations [mean (SD)/range, lg wet wt] in Antarctic invertebrates (a 5—7 cm; b 3—4 cm; m.i.g. middle intestinalgland)

Species St (n) Tissue Cadmium Zinc Copper

Parborlasia corrugatus 1 (2) Whole 0.40 33.00 0.600.30—0.50 31.00—35.00 0.30—0.90

2 (2) Whole 1.00 25.80 1.1523.80—27.80 1.10—1.20

Anthozoa 1 (1) Whole 0.20 149.00 0.60

Nacella concinna 1 (2) Foot 2.28 8.50 1.151.65—2.91 8.48—8.51 0.85—1.45

m.i.g. 4.45 36.76 16.974.00—4.89 36.24—37.27 14.40—19.54

5 (2) Foot 1.79 8.59 1.411.57—2.00 8.08—9.09 1.08—1.74

m.i.g. 5.14 31.62 16.554.14—6.14 27.33—35.19 14.68—18.42

7 (8) Foot 1.21 (0.8) 11.05 (2.30) 0.63 (0.44)0.21—2.51 6.40—13.87 0.50—0.81

m.i.g. 3.55 (1.04) 36.09 (6.64) 4.32 (0.39)2.01—5.50 22.85—43.59 3.90—5.12

8 (14) Foot 1.47 (0.84) 7.91 (2.23) 0.99 (0.33)0.74—2.60 4.23—11.70 0.55—1.36

m.i.g. 5.87 (2.08) 32.51 (5.95) 4.97 (1.00)3.33—10.22 24.43— 46.12 3.41—6.95

¹rophon brevispira 1 (6) Foot 2.30 (1.20) 22.12 (1.51) 30.61 (10.81)1.36—3.75 19.46—23.27 23.63—49.70

Nudibranchia 2 (1) Foot 0.90 74.00 0.80NDSipuncula 1 (1) Whole 0.47 69.87 14.64¼aldeckia obesa 3 (2) Whole 4.29 16.34 14.89

4.15—4.43 14.76—15.01

Glyptonotus antarcticus 3 (2) Whole 4.55 30.51 21.403.70—5.40 26.00—35.05 17.83—25.02

Odontaster validus 1 (6) Arm 14.71 (4.2) 24.20 (2.80) 8.92 (1.02)10.07—20.43 21.54—28.40 7.44—10.13

7 (2) Arm 15.03 22.19 8.6814.46—15.60 19.27—25.12 8.12—9.23

Neomilaster georgianus 1 (6) Arm (a) 0.47 (0.15) 13.20 (2.11) 3.70 (0.21)0.26—0.67 10.72—16.10 3.31—3.93

Arm (b) 1.08 (0.15) 20.42 (1.09) 9.21 (2.01)0.85—1.30 18.15—22.48 7.39—12.69

3 (6) Arm (a) 0.53 (0.12) 16.70 (2.00) 8.70 (6.01)0.41—0.68 12.83—19.71 3.10—14.37

7 (2) Arm (a) 0.71 12.64 1.800.53—0.82 6.52—18.15 0.85—3.32

Sterechinus neumayerii 1 (6) Gonads 0.48 (0.10) 37.30 (13.50) 2.51 (0.81)0.25—0.52 18.36—56.11 1.24—3.29

3 (1) Gonads 0.80 46.80 2.40

Ophiacantha antarctica 4 (2) Arm 0.84 27.98 0.920.80—0.88 25.40—29.70 0.84—0.99

the majority of the studied organisms, Zn and Cu levelswere higher than those of Hg and Cd.

The levels of metals analysed in the fish Nototheniacoriceps are shown in Table 5. They were in orderZn'Cu'Hg, while Cd values were below the detec-tion limit of the method. Metal levels differences be-tween sexes were not observed. The P-values of theANOVA were: Hg 0.040, Cd 0.221, Zn 0.337 and Cu

0.087. Neither was an increase of metal levels with bodyweight observed: Hg r"0.09, Cd r"2.50]10~3, Znr"0.12 and Cu r"!0.10.

Heavy metal contents in muscle, liver and eggs ofseveral bird species are shown in Figs. 2,3 and 4, re-spectively. Concentrations of essential and non-essen-tial metals were the highest in liver, followed by muscleand eggs. The greater sheatbill (Chionis alba) and

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Table 5 Heavy metal concentrations [mean (SD)/range, lg/g wet wt] in muscle of Notothenia coriceps (1 male; 2 female)

Species St (n) Sex Weight Mercury Cadmium Zinc Copper(g)

Notothenia coriceps 6 (11) 1 183—641 0.05 (0.03) (0.05 4.67 (2.55) 0.30 (0.14)0.01—0.10 1.00—6.70 0.04—0.50

6 (17) 2 80—773 0.05 (0.03) (0.05 3.57 (2.47) 0.27 (0.12)0.01—0.09 2.00—5.40 0.05—0.40

Fig. 2 Heavy metal concentrations (mean, lg/g wet wt) in muscle ofAntarctic seabirds

Fig. 3 Heavy metal concentrations (mean, lg/g wet wt) in liver ofAntarctic seabirds

blue-eyed shag (Phalacrocorax atriceps) showed higherlevels of Hg and Cu in muscle and Hg, Zn and Cu inliver than those found in penguins. Only the eggs ofAntarctic tern (Sterna vitatta) and the kelp gull (¸arusdominicanus) showed Hg levels above the detection

Fig. 4 Heavy metal concentrations (mean, lg/g wet wt) in eggs ofAntarctic seabirds

limit and presented the highest concentrations of Cd,Zn and Cu.

The highest concentrations of total mercury andcadmium in the Antarctic fur seal (Arctocephalus ga-zella) were found in liver and kidney, respectively. Inthese tissues, Zn and Cu levels were the highest andthey were similar (Table 6). The southern elephantseal (Mirounga leonina), unlike Arctocephalus gazella,showed concentrations of total mercury and cadmiumin muscle above the detection limit.

Discussion

Algae from the Antarctic ecosystem are important ele-ments of the littoral benthos during summer; the longdaylight hours and high nutrient concentrations avail-able favour their development. So they are becominga very important source of food to many Antarcticorganisms. Macrophytes accumulate only dissolvedmetals, reflecting the concentration of biologicallyavailable metals, and therefore they are used as anindicator of heavy metal levels in seawater. Honda et al.(1987) found the relation Cd'Hg in Antarctic sea-water, with values significantly below the algae levels

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Table 6 Heavy metal concentrations [mean (SD)/range, lg/g wet wt] in Antarctic marine mammals (males)

Species St (n) Tissue Mercury Cadmium Zinc Copper

Arctocephalus gazella 6 (4) Muscle (0.05 (0.05 20.30 (5.60) 1.30 (0.20)12.70—25.70 1.10—1.50

Liver 5.50 (1.50) 2.90 (1.00) 30.40 (6.20) 14.40 (2.00)4.10—7.60 1.90—3.50 25.30—38.40 11.90—16.20

Kidney 0.25 (0.06) 4.80 (0.90) 30.00 (6.40) 13.70 (6.10)0.20—0.30 3.70—5.90 23.80—38.90 8.40—22.30

Fat (0.05 (0.05 7.00 (2.60) 0.40 (0.20)3.20—8.40 0.20—0.60

Mirounga leonina 1 (2) Muscle 0.18 0.09 26.48 0.630.17—0.19 0.05—0.12 24.37—28.58 0.57—0.68

Skin 0.12 (0.05 27.90 0.510.09—0.14 25.07—30.72 0.49—0.52

Fat (0.05 (0.05 0.57 1.000.30—0.84 0.54—1.46

Table 7 Heavy metal concentrations (lg/g dry wt) in algae from other areas (Nd non detectable; NA not analysed)

Taxon Mercury Cadmium Zinc Copper Area Source

Phaeophyta 0.007—0.32 0.19—0.73 1.30—12.40 0.74—3.50 Great Barrier Denton andReef Burdon-Jones (1986)

Rodophyta Nd-0.167 0.21—2.20 3.30—22.80 1.20—5.60 Great Barrier Denton andReef Burdon-Jones (1986)

Chlorophyta Nd-0.246 0.08—1.70 1.70—17.00 1.00—6.20 Great Barrier Denton andReef Burdon-Jones (1986)

Phaeophyta NA 0.50—1.60 11.00—82.00 2.80—25.10 Hong Kong Ho (1987)Rodophyta NA 0.30—2.80 11.00—212.00 3.60—81.70 Hong Kong Ho (1987)Chlorophyta NA 0.30—1.20 17.00—310.00 6.90—271.00 Hong Kong Ho (1987)

reported in the present paper. Also algae levels fulfil thesame relationship between these metals, Cd'Hg.

The levels obtained varied a great deal from speciesto species and from one area to another, thus notsuggesting a clear pattern of accumulation betweengroups. Red algae did not show concentrations of Cdhigher than the green or brown algae, unlike the trendobserved by Denton and Burdon-Jones (1986). In addi-tion, the levels of Zn and Cu were substantially lowerthan those reported for metal-polluted areas like HongKong (Ho 1987) and similar to those from pristineareas, such as the Great Barrier Reef (Denton andBurdon-Jones 1986). Nevertheless, Cd values in Ant-arctic algae were higher than those from pristine areasand of the same order as its impacted areas, whichmight be due to the upwelling of cadmium-enricheddeep waters (Honda et al. 1987). Literature values forCd, Cu, Zn and Hg in algae are given in Table 7. Alamand Sadiq (1993) found the highest mean concentrationof Cd in Antarctic sediments from Jubany, which alsohad high concentrations of Zn and Cu. The high con-centrations of metals found in algae from the same areacould be due to the metal content in seawater and alsoto the accumulation capacity of each species.

Suspension-feeding invertebrates (bryozoans, sponges,brachiopods and ascidians) accumulate contami-nants from water in dissolved and particulate forms.In Antarctica, this group is located under the seaice during the winter season, only receiving smallamount of food (winter oligotrophy). It seems thatthese invertebrates survive during winter in a state ofvegetative life, with the aid of the reserves they haveaccumulated during the months of eutropy (Arnaud1977). Taking into account the high Cd concentrationobserved only in porifera and brachiopoda, a potentialCd accumulation mechanism in these groups seems tobe probable.

Sedentary polychaetes take metals up from sedimentparticulates, interstitial water and infaunal species.Sediments generally contain higher concentrations ofheavy metals than aquatic organisms. Consequentlysediment-feeding organisms like polychaetes exhibithigher metal concentrations than do other suspensionfeeders. However, in the different invertebrates sam-pled, only Zn concentrations were higher.

Apart from the groups already mentioned, otherinvertebrates with higher trophic levels were alsostudied. The values of Sipuncula, Nudibranchia and

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Table 8 Heavy metal concentrations (lg/g dry wt) in some invertebrates from other areas (NA not analysed)

Taxon Cadmuim Zinc Copper Area Source

CrustaceaGlyptonotus 0.98—1.20 60.60—66.50 133.00—165.00 Antarctica Petri and Zauke (1993)antarcticus¼aldeckia obesa 1.17—1.89 267.00—335.00 72.80—88.70 Antarctica Petri and Zauke (1993)G. antarcticus 1.91 88.70 54.40 Antarctica Rainbow (unpublished data)

in Petri and Zauke (1993)¹hemisto 8.00—118.00 NA 20.00—875.00 Antarctica Henning et al. (1985) ingaudichaudii Schulz-Baldes (1992)¹. gaudichaudii 18.70—52.60 NA 28.10—31.10 Antarctica Rainbow (1989)¹. compressa 69.50 76.30 38.60 NE Atlantic Rainbow (1989)

AnthozoaActinia equina 0.032—0.38 87.00—227.00 NA English coast Harland et al. (1990)Anemonia viridis 0.028$0.006 116.00$10.00 NA English coast Harland et al. (1990)

Actiniaria were the highest found among the inver-tebrates. In the latter, the level was in the range ob-served by Harland et al. (1990) in Actinia equina (Table8). These authors suggested that Zn is assimilated bythe gastrodermal tissue, whereas the carnivorous diet ofAntarctic anemones could be a source for Zn uptake.

The amphipods have been recognized as bioconcen-trators of heavy metals in the marine environment,particularly in the case of Cd, which may be due tofeeding habits or a consequence of a strong physiolo-gical affinity for the metal (Hamanaka and Ogi 1984;Rainbow 1989). Our values for Cd in ¼aldeckia obesa(Table 4) are lower than those reported in amphipodsby Rainbow (1989), but significantly higher than thosefound in the same species by Petri and Zauke (1993)(Table 8). These great differences, also evident in Glyp-tonotus antarcticus, may be due to differences in bodysize of the animals sampled. In this relation, Hamanakaand Ogi (1984) showed a significant positive correlationbetween Cd concentration and body size in the hy-periid amphipod Parathemisto libellula.

In the molluscs Nacella concinna and ¹rophonbrevispira, very high levels of Cd were found, not onlyin the middle intestinal gland (m.i.g.) but, surprisingly,also in muscle. The presence of metallothioneins asa mechanism of Cd detoxification in the muscular tis-sue of molluscs, suggested by Noel-Lambot et al.(1980), provided possibilities of Cd accumulation in thistissue. The origins of this level could be the strictlyherbivorous and carnivorous habits of Antarctic lim-pets and snails, respectively.

Odontaster validus, the most abundant starfish on theAntarctic shelf, had the highest Cd level among inver-tebrates. Arnaud (1977) reported that this species util-izes the widest range of food items and types of feedingbehaviour of any Antarctic asteroid. Moreover, the lowpressure of predation on certain species, like O. validus,determined that it may live more than 100 years. Thestrong Cd bioaccumulation in this species may be dueto its longevity, rather than to availability of Cd in the

diet. Moreover, den Besten et al. (1989) reported thepresence of metallothionein-like proteins in the sea starAsterias rubens, which can accumulate Cd at highlevels. However, the starfish Neomilaster georgianus, anopportunistic predator and scavenger of the subtidalbenthic communities, showed a lower Cd level than O.validus. Negative correlations of Zn, Cd and Cu withbody size were observed in N. georgianus as shown inother benthic organisms (Boyden 1974; Hornung andOren 1980/1981). This correlation was attributed toa higher growth rate and faster metabolism in theyounger and smaller organisms than in older ones, aswell as higher surface absorption in the former animals(Hornung et al. 1991). Gonzalez et al. (1991) suggestedthat gonads are important Zn accumulators in marineorganisms. The high level found in our samples of thesea urchin Sterechinus neumayerii confirmed this trend.

Top predators have been considered to be effectivebioaccumulators and biomagnificators. Thus, theyhave been widely utilized as biomonitors of variouspollutants in the marine environment.

The notothenid Notothenia coriceps is an omnivor-ous fish with a wide trophic spectrum, which is com-posed of benthic and pelagic organisms, and its metalconcentrations in muscle nearly agree with those of thepelagic Antarctic fish Pagothenia borchgrevinki studiedby Honda et al. (1983). Both species have in commonthe krill (Euphausia superba) as the most importantfood item in late spring and summer. These authors didnot find differences of metal concentration between thesexes like those found in Notothenia coriceps, in thisstudy although the metal levels of the latter did notvary with body weight. In Pagothenia borchgrevinki theconcentrations of Zn and Cu were inversely propor-tional to body weight, while the relationship was posit-ive for Cd and Hg.

The Antarctic fur seals (Arctocephalus gazella) fromthe South Orkney Islands, like other marine mammals,accumulated the highest level of mercury in the liver,while for cadmium there were relatively high levels in

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the liver and kidney (Wagemann and Muir 1984). Cd,Zn and Hg concentrations in the liver of males (Table 6)were considerably lower than those reported in femalesof the same species from Bird Island, South Georgia(Malcolm et al. 1994). In comparison with other sealspecies, these concentrations were also lower thanthose of South American fur seal (Arctocephalus austra-lis) males from the Uruguayan Islands (Gerpe et al.1990) and southern elephant seal (Mirounga leonina)from Antarctica. The Antarctic fur seal feed almostexclusively on krill during summer (Daneri and Coria1992), which have a high level of Cd (Honda et al. 1987;Yamamoto et al. 1987) and would be the immediatesource of this metal. The accumulation of Cd in liverand kidney of mammals is related to its selective stor-age or sequestration by metallothionein, without signsof toxicity (Wagemann and Muir 1984). However, bothArctocephalus australis and Mirounga leonina eat main-ly fishes, and cephalopods represent a small proportionof the diet (Laws 1977; Vaz-Ferreira and Ponce deLeon 1987). This accounts for the lower bioaccumula-tion factor of Hg and Cd in the Antarctic fur seal, inrelation to South American fur seals and southernelephant seals. In the case of mercury, some detoxifica-tion of this metal within tissues (liver and kidney)results from the interactions with selenium and metal-lothioneins and from the formation of granules withinhepatocytes in marine mammals (Andre et al. 1990)reflecting the existence of the low mineralization pro-cess leading to the storage of inorganic Hg, mainly inthe liver (Joiris et al. 1991). In general there was con-siderable individual variability in liver Cd and Hgconcentrations, which can be attributed to age, bodysize and sex in marine mammals (Malcolm et al. 1994).The analysis of the essential metals showed high valuesin liver and kidney of both fur seals (Arctocephalusgazella and A. australis). It has been suggested that inmarine mammals homeostatic control of Cu and Znmay be mediated by metallothioneins (Muir et al.1988). The concentrations of both metals in liver ofArctocephalus gazella were within a range in which thisregulation is active in mammals: 20—100 ug/gwwt forZn and 3—30 ug/gwwt for Cu (Law et al. 1991).

Birds, like mammals, are useful biological indicatorsof heavy metal pollution in the environment because oftheir wide distribution and high trophic level. Differ-ences in metal contents between species may presum-ably reflect differences in feeding habits more thanmetabolic differences (Honda et al. 1990; Hunt et al.1981; Ogi 1986 in Honda et al. 1990). Adelie (Pygoscelisadeliae) and gentoo (Pygoscelis papua) penguins areabundant and important components of the upper Ant-arctic food web, feeding mainly on krill and secondarilyon fishes and amphipods (Croxall and Lishman 1987;Lishman 1985). Adelie penguins have concentrations indifferent tissues and in eggs in agreement with thosefound by Honda et al. (1986). Compared with pelagicseabirds from the North Pacific (Honda et al. 1990),

Fig. 5 Cadmium concentrations (mean, lg/g wet wt) in variousAntarctic organisms: 1 Euphausia superba (whole) after Honda et al.(1987); 2 filter feeders (whole), Porifera, Brachiopoda, Bryozoa, Dis-taplia cylindrica, Polychaeta; 3 Nacella concinna; 4 invertebrates(whole), Parborlasia corrugatus, Anthozoa, ¼aldeckia obesa, Glyp-tonotus antarcticus, Odontaster validus, Neomilaster georgianus,Ophiacanta antarctica (muscle), ¹rophon brevispira, Nudibranchia;5 Notothenia coriceps; 6 birds (liver), Pygoscelis adeliae, Chionisalba, Phalacrocorax atriceps; (muscle), Pygoscelis adeliae, Pygoscelispapua, Chionis alba, Phalacrocorax atriceps; 7 Arctocephalus ga-zella; 8 Mirounga leonina

Fig. 6 Zinc concentrations (mean, lg/g wet wt) in various Antarcticorganisms. For species see Fig. 5

penguins have mercury concentrations 1 order of mag-nitude lower, but higher Cd levels. Lower Hg levels inmuscle probably occur because their food prey usuallyhave low Hg concentrations. Moreover, and similarlyto other birds, penguins concentrated Hg in featherspreferentially to any other tissue. The greater sheatbill(Chionis alba) eats human kitchen refuse, algae, eggs,penguin chicks, bird and mammal excreta and car-casses and seal placenta (Favero 1994). However, fishes,followed by benthic organisms such as polychaetes,

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Fig. 7 Copper concentrations (mean, lg/g wet wt) in various Ant-arctic organisms. For species see Fig. 5

gastropods, bivalves, cephalopods and crustaceans areknown to be the main components of the blue-eyedshag (Phalacrocorax atriceps) diet (Coria et al. 1996).The concentrations of mercury and cadmium in thesespecies were higher than those found in penguins.Probably the difference is that these penguin specieshave an Antarctic distribution, whereas Chionis albaand Phalacrocorax atriceps also reach the SouthAmerican coast (Watson 1975). As a consequence ofthis, they must feed in both pristine and non-pristineareas. The same differences between penguins, sheat-bills and shags, mentioned for non-essential metals,were found in essential metals, although the latter aremetabolically regulated in seabirds (Muirhead andFurness 1988). The metal distribution in tissues of birdswould result from their uptake, storage and eliminationproperties. In the last process feathers have an impor-tant role in mercury detoxification. Birds take up mer-cury from their food and much of it goes into theirplumage during feather growth (Furness et al. 1986)and can also be transferred to eggs, particularly themethylmercury (Lewis and Furness 1993; Ohlendorfand Fleming 1988; Thompson et al. 1990). The high-est levels of cadmium, mercury and zinc in eggs ofSterna vitatta (ichthyophagous) and ¸arus dominicanus(which feeds mainly on limpets) may be indicative ofthe higher trophic level of these species, compared withpenguins and blue-eyed shags.

The biomagnification process of organic mercurydepends upon the food web, and high trophic levelanimals have a higher content that lower trophic levelones (Waldichuck 1985). A low level biomagnificationof mercury in analysed biota was found when wecompared mercury concentrations of algae and inver-tebrates below the method detection limit and verte-brates’ muscle tissues. However, Cd (Fig. 5), Zn (Fig. 6)and Cu (Fig. 7) showed species- and metal-specific ac-

cumulation, but not biomagnification, in both Antarc-tic vertebrates and invertebrates.

The data presented here are representative of a pris-tine environment and will be of value when assessingthe future impact of anthropogenic developments with-in Antarctica. The study also permits the selection andrecommendation of a candidate species for continuedmonitoring studies in the area.

Acknowledgements The authors are grateful to D. Leva, Dr. G.Ferreyra, Lic. L. Ricci, Lic. J.M. Ageitos, A. Malaspina, Lic. D.Rodrıguez and Lic. M. Favero.

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