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Home , Biomagnification, Paramoera walkeri, South polar skua, Terra Nova (ship)

MARINE PROGRESS SERIES Vol. 169: 65-76.1998 1 Published August 6 i Mar Ecol Prog Ser

Biomagnification of in an marine coastal

R. Bargagli*, F. Monaci, J. C. Sanchez-Hernandez, D. Cateni

Department of Environmental Biology, University of Siena. Via delle Cerchia 3, 1-53100 Siena, Italy

ABSTRACT. Total 1lg concentrations were determined in marine sedlments and biota from the inner shelf of (). Like published data on air, snow and soils from the same region, Hg levels in the finest fraction of marine sediments were among the lowest ever reported for coastal marine environments (0.012 r 0.007 pg g-' dry wt). A progressive increase in Hg concentrations was found in organisms at different levels of the (phytoplankton < zooplankton and ben- thic primary consumers < detritivorous and opportunistic benthic invertebrates < eplpelagic fish < dem- ersal fish and plankton-feeding seabirds < fish-eating penguins < predatory birds and Weddell seal). In general, primary producers and consumers showed slightly lower Hg concentrations (0.076 * 0.023 pg g-l dry wt) than organisms of related from other seas, but values in feathers (2.91 + 1.93 pg g-' dry wt) of the Antarctic and in tissues of a MIeddell seal (44.0 and 24.0 pg g-l dry wt in the liver and spleen, respect:vely) WC:? s:milar to those in and sedls from the northern hemmsphere. Trophic connections between organisms in well developed benthic communities, phytoplankton and fish and environmental factors such as enhanced upwelling of cold water, sea ice and low light are deemed to enhance natural biomagnification processes of Hg in the pristine Antarctic coastal environment.

KEYWORDS: Mercury Sediments Coastal food web - Biomagnification Ross Sea - Antarctica

INTRODUCTION atmospheric deposition over the past 34000 yr and emission of gaseous mercury by oceans has been Antarctic have unique characteristics recognised as the principal source of the metal in the resulting from a long evolutionary history under Antarctic continent (Vandal et al. 1993). In Victoria extreme environmental conditions. Until recently, they Land the lowest mercury concentrations ever reported were protected from heavy human impact by their have been measured In snow (Sheppard et al. 1991), remoteness and inhospitality They therefore consti- air (de Mora et al. 1993) and soil (Bargagli et al. 1993). tute a natural laboratory where biogeochemical cycles In contrast to the relatively abundant data on envi- of metals can be studied under relatively unpolluted ronmental abiotic matrices, very little is known of mer- environmental conditions. cury concentrations in Antarctic terrestrial and aquatic Despite formidable technical and logistic difficulties, biota. Better knowledge of Hg accumulation in marine improvements in analytical and ultra-clean sampling organisms at different positions in the food web is techniques in the last decade have led to a better important because biomagnification in the aquatic understanding of the environmental distribution and food web is a well known process (D'Itri 1991) and cycling of metals in Antarctica (Boutron & Patterson most of the Antarctic is concentrated in the 1986, Wolff 1990). With regard to mercury, Antarctic marine environment. Data on mercury levels in ice-core analyses have provided a reconstruction of Antarctic marine organisms mainly regard species at the top of the food web, such as penguins or marine mammals (McClurg 1984, Honda et al. 1986a, b, Yamamoto et al. 1987a, Szefer et al. 1993). Moreover,

0 Inter-Research 1998 Resale of full article not permitted 66 Mar Ecol Prog Ser 169 65-76, 1998

these data are not unequivocal as differences up to 1 Sampling of higher vertebrate species was planned order of magnitude have been reported for similar tis- so as to avoid death or significant . On the sue or organs from the same or closely related around Terra Nova Bay, eggs, primary feathers, specles. For example, Honda et al. (1986a) found an chick plumage and guano samples were gathered average mercury concentration of 0.007 pg g-' (wet wt) when possible in abandoned nests of snow petrels in muscle of the Adelie penguin Pygoscelis adeliae, Pagadroma nivea, Antarctic skuas Catharacta mac- whereas Szefer et al. (1993) reported a mean value of cormicki, Adelie penguins Pygoscelis adeliae and 0.660 pg g-' (dry wt). Even the most recent data on emperor penguins Aptenodytes forsteri. Samples of mercury concentrations in some marine invertebrates stomach contents were taken from 5 Adelie penguins and fish contain discrepancies. Much lower Hg con- breeding at Edmonson Point (74" 21' S, 165" 10' E) by centrations have been reported for organisms collected the water off-loading. Vanous internal organs and tis- along the Antarctic Peninsula (Palmer Locarnini & sues were obtained from an Adelie penguin acciden- Presley 1995, de Moreno et al. 1997) than in Victoria tally snared in a trammel net and an adult female Wed- Land (Minganti et al. 1994). This is rather surprising dell seal Leptonychotes weddellii (weight = 330 kg) because the latter is more remote and less frequented found dead on the Terra Nova Bay coast. by humans. To reduce contamination, samples were always han- The main objectives of this study were to investigate dled with disposable gloves, very clean plastic Hg transfer and biomagnification in the marine food or stainless steel tools, and placed in individual sealed web and the ecological factors involved in these pro- polythene bags and frozen for storage and transport to cesses. Mercury concentrations were determined in Italy. recent marine sediment and a large spectrum of organ- Sample preparation and mercury analysis. In the isms with different , positions in the food web laboratory, sediment samples were freeze-dried and and feeding habits from the inner continental shelf at then sieved through a 125 pm stainiess sreei screen. Terra Nova Bay (Ross Sea, Antarctica). Composite samples of phytoplankton (mainly diatoms

MATERIALS AND METHODS

Study area and sampling. Samples were collected during the 5th and 6th Italian Antarctic Expeditions (austral summers 1989/90 and 1990/91) at Terra Nova Bay (northern Vlctoria Land; Fig. 1).Surface sedi- ments and organisms were collected on the inner continental shelf (from 74" 40' S to Ross 74" 50's) at depths ranging from 5 to 300 m, except for krill Euphausia superba samples Sea which were collected in the open Ross Sea (from 72" to 75" S and 170" and 178" E). Twenty samples of surface sedirnents (the top 3.0 cm) were taken on soft bottoms (from 20 to 300 m depth) with a stainless steel box corer. Samples were scooped from the centre of the box with a plastic spatula. Phytoplank- ton and were sampled with coni- cal nylon nets (1 m in diameter, 50 and 500 pm mesh size, respectively), towed just below the surface. Krill samples were collected in the Ross Sea with a plankton sampler (EZNET BIONESS) equipped with 10 nets of 250 and 500 pm mesh size at a depth ranging from l0 to 100 m. Benthic organisms were obtained w~tha Van Veen grab or by dredging on hard bottoms. Fish specimens were caught with a trammel net or baited long lines. :ig. 1 hfap showing the study area and sediment sampling points (0) Bargagli et al.: Biom agnification of mercury 67

of the genera Nitzschia and Chaetoceros), seaweeds RESULTS Iridaea cordata, zooplankton (mainly the copepods Metridia gerlachei and Euchaeta antarctica), sponges The fine fraction (1125 pm) of surface sediments (belonging to the genera Rossella, Tedania and Axo- from Terra Nova Bay had an average Hg concentration ciella), ascidians, the common amphipod (+SD) of 0.012 + 0.007 pg g-' dry wt (range 0.006 to walkeri and the polychaete Harmothoe spinosa were 0.027 pg g-' dry wt). Values were always much lower freeze-dried. All the other organisms, the bivalve than the Hg concentration (0.050 pg g-I dry wt) sug- molluscs Laternula elliptica and Adamussium col- gested as background level for unpolluted marine sed- becki, the gastropod Neobuccinum eatoni, the sea iment~(Sadiq 1992). No significant increase was found urchin Sterechinus neumayeri, the sea star Odonaster in samples collected close to the Italian scientific sta- validus and fish belonging to the Trematon~us tion of 'Baia Terra Nova'. Concentrations of TOC (T bernacchii, T. hansoni, T. newnesi) and icefish ranged from 0.20 to 0.55 % and no significant relation- Chionodraco hamatus, were thawed, identified as to ships with those of Hg were found. genus or species, and body length and other basic Average Hg concentrations (Table 1) progressively morphometric parameters recorded. Whenever possi- increased in the order phytoplankton < zooplankton < ble muscle, liver (or the digestive gland), gills, kid- krill. Because Hg values in zooplankton had a CV of ney, soft tissue and gonads were removed and 47.5% (probably due to different proportions of the lyophilised. Prior to the analytical determinations, various phyla in samples), a statistically significant dif- feathers were carefully cleaned of loosely attached ference (Mann-Whitney U test, p < 0.05) was only material and each egg albumen separated and found between Hg concentrations in phytoplankton freeze-dried. Sediment samples were vacuum-dried and krill. Comparisons with literature data on plankton and then passed through a 125 pm stainless steel from other seas were made difficult by differences in sieve to reduce the effects of grain-size variations on sampling methods and phyla composition. Fowler Hg concentrations. (1990) assumed a Hg concentration of 0.100 pg g-l dry A subsample (0.15 g) of homogenised superficial wt (i.e. twice the overall average content of 0.059 ? sediment and biological material was decomposed 0.033 py dry wt in Antarctic diatoms and copepods) with concentrated HN03 (Merck Suprapur) in Teflon as background level for mixed plankton samples from vessels under pressure at 120°C for 8 h. Mercury was different seas around the world. The average Hg con- determined in the digested solution by Flow Injection centration in krill samples from the Ross Sea was close Atomic Absorption Spectrometry (FIAAS) using a to the lower limit of the range (0.028 to 0.497 1-19 g-' dry Perkin Elmer FIMS 400. Hg determinations were wt) reported by Fowler (1986) for euphausiids from dif- based on 3 replicates. The precision of Hg determina- ferent oceans. However, the data in Table 1 are 2 to tion~, expressed as the coefficient of variation on 3 times higher than those reported for krill samples col- repeated assays of the same sample, was about 5%. lected on the opposite side of the : The minimum detection limit in pg g-' dry wt was 0.035 pg gm' dry wt in the Drake Passage (Yamamoto et 0.005. Each series of analysis was accompanied by al. 1987b) and 0.025 pg g-' dry wt off the Western concurrent mineralisation and determination of Stan- Antarctic Peninsula (Palmer Locarnini & Presley 1995). dard Reference Materials (SRMs) no. 1646 'Estuarine The results of Hg determinations in the widespread Sediment' and no. 1577 'Bovine Liver' from NIST seaweed Iridaea cordata showed wide variations (Gaithersburg, USA). Batches with accompanying (approximately 1 order of magnitude), probably due to SRMs outside the certified range were repeated. The different contributions of epibiota on the foliaceous recovery rate ranged from 86 to 109%, the average thalli (Table 1). The range of Hg concentrations in I. being 92 % for sediments and 96 % for biotic samples. cordata was similar to that previously found in other Subsamples of superficial sediment were analysed for Rhodophyta species from the Great Barrier Reef (unde- total organic carbon (TOC) content by a modified tectable to 0.167 pg g-' dry wt; Denton & Burdon-Jones Walkley-Black titration method (Gaudette et al. 1986). High variability in Hg concentrations was also 1974). found among the benthic invertebrates analysed, Nonparametric statistical tests (Ma.nn-Whitney U probably reflecting marked differences in , test) were used to detect significant differences be- and feeding habits. The total body content of tween groups. Pearson's correlation coefficients were mercury increased from organisms feeding mainly on also calculated for the relationship between mercury diatoms, such as the amphipod Paramoera walkeri and concentration and body weight. A probability level of sponges, to those feeding on and/or (e.g. 0.05 was taken as significant. All statistical analyses ascidians, sea urchins and holothurians) and to more were performed using the Statistics programme (Stat- omnivorous opportunistic feeders (e.g. scavengers and Soft Inc.). predators such as brittle stars and sea stars). The high- 68 Mar Ecol Prog Ser 169: 65-76, 1998

Table I. Mrrcury concentrations (pg g" dry wt) in invertebratesfrom Terra Nova Bay (RossSea, Antarctica)

Taxon Species Tissue n Mean + SD Min.-max

Phytoplankton Pooled across species Zooplankton Pooled across species Krilld Pooled across species Rhodophyta Iridaea cordata Whole Porifera Pooled across species Whole Ascidiacea Pooled across species Whole Echinodermata Holothuroidea Pooled across species Whole Ophiuroidea Pooled across species Asteroidea Odontaster validus Arms Soft tissue Gonads Echinoidea Sterechinus neuma yen Soft tlssue Gonads Annelida Harmothoe spinosa Whole Crustacea Paramoera walkeri Whole Pycnogonida Colossendeis a ustralis Whole Mollusca Bivalvia Adamussium colbecki Muscle Digestive gland Gonads Gills Muscle Digestive gland Gonads Gills Prosobranchia Neobuccinum eatoni Muscle Digestive gland Gonads

aKrill samples were collected in the open Ross Sea

est Hg levels were recorded in gills of filter-feeding proposed as a suitable biomonitor to detect environ- benthic molluscs, especially those of the Antarctic scal- mental changes in metal bioavailability in Antarctic lop Adamussium colbecki. coastal waters (Berkman & Nigro 1992).Minganti et al. Data on Hg concentrations In benthic organisms (1995) reported Hg concentrations ranging from 0.132 from the Southern Ocean are scarce. In a survey by de to 0.372 ug g-' dry wt in the soft tissue of A. colbecki Moreno et al. (19971, a large number of species col- collected each summer from 3.987 to 1992 at Terra lected from different sites off the Antarctic Peninsula Nova Bay. were analysed for Hg. The authors were unable to Total Hg concentrations in muscle, liver, kidney, gills detect Hg even in invertebrates such as the and gonads of the most common fish species in the study gastropod Trophon brevisplra and the giant isopod area are surnmansed in Table 2. Trematomus bernacchii Glyptonotus antarcticus. Unfortunately only wet tis- and Trematomus hansoni showed significantly (p< 0.01, sues were analysed and the detection limit (0.05pg g-1 Mann-Whitney U test) higher concentrations of Hg in wet wt) was probably too high for detecting the low muscle and organs than Trematomus newnesi and the levels, typical of Antarctic ecosystems. There is also icefish Chionodraco hamatus. Fig. 2A shows average evidence that Antarctic benth~cinvertebrates, espe- values of Hg measured in muscle, liver and kidney of T cially molluscs, accumulate metals (Mauri et al. 1990, bernacchii and those previous1.y reported for this species Nigro et al. 1997) and Adamussium colbecki has been from Terra Nova Bay continental shelf (Minganti et al. Bargag11 et al.. Biomagnificatlon of mercury 69

Table 2. Mercury concentrations (pg g dry wt) in fish of the genus Trematomus and in the icefish Chlonodraco hamatus from Terra Nova Bay continental shelf

Species Length (cm) Weight (g) Tissue Mean * SD

T bernacchii 17-28 83-354 Muscle 0.83 t 0.65 Liver 0.46 i 0.25 Kidney 0.94 * 0.64 Gills 0.34 * 0.17 Gonads 0.26 * 0.14 T hansoni 23-32 147-340 Muscle 0.47 + 0.32 Liver 0.23 +0.16 Kidney 1.06 i 0.46 Gills 0.44 i 0.28 Gonads 0.20 * 0.12 T. newnesi 20-25 89-194 Muscle 0.29 + 0.24 Liver 0.16 + 0.09 Kidney 0.27 + 0.15 Gills 0.06 * 0.02 Gonads 0.19 * 0.08 C. hamatus 33-39 270-615 Muscle 0.34 i 0.33 Liver 0.19 * 0.12 Kidney 0.28 + 0.20 Gills 0.14 + 0.09 Gonads 0.21 + 0.09

1994).According to Capelli et al. (1990),concentrations of Hg ifi fish muscle wcrr significantly correlated (r = 0.81, p < 0.01) with body weight (Fig. 2B). The accumulation of Hg in breeding along was evaluated by an indirect non- destructive approach (Table 3). Concentrations of Hg in feathers, eggs and chick plumage of the south polar skua were 3 to 6 times higher than those measured in the same biological materials of snow petrels and pen- guins. Samples collected in the colony at Cape Washington always had higher concen- trations of total Hg than samples from Adelie penguin rookeries on the Terra Nova Bay coast. Although comparisons with literature data on Hg levels in feathers of related species from other seas are made difficult by factors such as differences in lifespan and moulting strategies (Stewart et al. 1997), Hg concentrations in snow petrels breeding in north- ern Victoria Land were much lower than those reported for other petrel species (e.g. Pterodroma lessonii and A4acronectes halli) from subantarctic islands (Lock et al. 1992). Emperor and Ad6lie penguin feathers also had a much lower content of Hg than 0.0 - . I I 1 those of blue penguins Eudyptula mjnor from New 0 100 200 300 400 500 Zealand (Table 3). In contrast, feathers and chick Weight (g) plumage of the Antarctic skua Catharactra mac- cormicki and Arctic skua Stercorarius parasiticus from Fig. 2. (A) Comparison between total Hg concentration In the Shetland Islands (60" 08' N, 2"05' W) had Hg con- muscle, liver and kidney of Trematomus bernacchii from the current study (white bar) and data from Minganti et al. (1994) centrations in the same range (Stewart et al. 1997). (shaded bar) (B) Relationship between total Hg concentra- Average Hg in stomach contents of Adelie penguins tions in muscle and body welght in this study (U) and data matched those in krill samples, whereas penguin tissues from Capelli et al. (1990) (m) 70 Mar Ecol Prog Ser 169: 65-76. 1998

showed increasing concentrations in the order testis < by Yamamoto et al. (1987a) in 2 Weddell seals from the brain < muscle < kidney i liver (Table 4). According to Syowa Station were lower than those in our specimen. published data on Pyqoscelis adeliae (Szefer et al. 1993), However, except for low concentrations reported for Eudyptula minor, Eudyptes crestatus and Eudyptes scla- muscle of Arctocephalus gazella (de Moreno et al. ten (Lock et al. 1992), Hg concentrations (dry wt) in pen- 1997) and liver of Ommatophoca rossi (McClurg 1984) guin liver range from 1.4 to 2.4 pg g-' irrespective of spe- and Phoca groenlandica (Skaare et al. 1994), the pre- cies and sampling area. The only exception was a lower sent values were in the same range as those reported concentration measured by Lock et al. (1992) in the liver for adult seals of other species in the southern and of a Fiordland crested penguin Eudyptes pachyrhyn- northern hemispheres (Table 5). chus. Although on a wet weight basis, the concentrations reported by Honda et al. (1986a) in Adelie penguins and by de Moreno et al. (1997) in muscle of the same species DISCUSSION are lower than all other data (Table 4). The highest mercury concentrations of the present Environmental distribution and bioavailability of Hg study were recorded in liver of the Weddell seal (44.0 pg g-' dry wt) found dead on the Terra Nova Bay Very low concentrations of total Hg were measured coast. Much lower concentrations were detected in in the finest fraction of recent marine sediments from sp!zcn, rr?csc!e and pancreas (Table 5). Although Terra Nova Bay. This result, together with previous expressed on a wet weight basis, the values reported findings for snow, air and soil (Sheppard et al. 1991,

Table 3. Mercury concentrations (pg g-' dry wt) in eggs, adult body feathers, guano and chick plumage from Terra Nova Bay seabirds. Literature data on related species is also reported for comparison

Species Region Sample- n Mean * SD Source Petrels Pagodroma nivea Terra Nova Bay Eggs" 3 0.59 t 0.08 This study Feathers 5 0.54 t 0.18 This study Pterodroma cooki Subantarctic Islands Feathers 1 12.4 Lock et al. (1992) Pterodroma lessonii Subantarctic Islands Feathers 1 24.4 Lock et al. (1992) Daption capense Subantarctic Islands Feathers 1 1.3 Lock et al. (1992) Macronectes halli Subantarctic Islands Feathers 1 24.0 Lock et al. (1992) Macronectes giganteus New Zealand Feathers 44 11.0 ? 6.1 Thompson et al. (1993) Skuas Catharacta maccormlcki Terra Nova Bay Eggsd 4 1.61 t 1.22 This study Feathers 7 2.91 t 1.93 This study Guano 6 0.22 + 0 10 This study Chick plumage 1 1 90 This study Catharacta skua Shetland Adult feathers 54 6.34 + 2.60 Stewart et al. (1997) Chick down 58 4.15 +_ 1.39 Stewart et al. (1997) Chick feathers 28 1.22 t 0.38 Stewart et al. (1997) Stercorarius parasiticus Shetland Adult feathers 28 2.52 + 2.23 Stewart et al. (1997) Chick down 36 2.00 * 0.91 Stewart et al. (1997) Chick feathers 30 0.46 * 0.22 Stewart et al. (1997) Penguins Pygoscelis adehae Terra Nova Bay Egg" 13 0.26 + 0.08 This study Feathers 3 0 82t0.13 This study Guano 7 0 17 * 0.10 This study Chick plumage 11 0.37 * 0.15 This study Stomach content 5 0.08 r 0 01 This study Pygoscelis adeliae Syowa station Feathers 10 0.17 * 0.04 Honda et al. (198613) Aptenodytes forsten Terra Nova Bay Feathers 3 0.98 * 0.21 This study Guano 5 0.31 t 0.03 This study Chick plumage 1 0.67 This study Eudyptula minor Subantarctic Islands Feathers 5 3.40 t 3.70 Lock et al. (1992)

dAlbumen Bargagli et al.. Biomagn~ficatlonof mercury 7 1

Table 4. Mercury concentrations (pg g-' dry wt) in tissues of an Adelie penguin compared with literature data on penguins from other Antarctic and subantarctic regions

Region Species n Mean + SD Source

Muscle Terra Nova Bay Pygoscelis adeliae 1 0.60 This study Antarctic Peninsula P. adeljae 5 0.63 Szefer et al. (1993) Antarctic Peninsula P. adeljae de Moreno et al. (1997) Syowa station P. adeljae Honda et al. (1986b) Antarctic Peninsula P. papua de Moreno et al. (1997) Liver Terra Nova Bay P adeliae This study Antarctic Peninsula P. adeliae de Moreno et al. (1997) P. adeliae Szefer et al. (1993) Bouvetaya Island P. antarctica Norheim (1987) Eudyptes chrysolophus Norheim (1987) Subantarctic Islands Eudyptula minor Lock et al. (1992) Eudyptes crestatus Lock et al. (1992) E. pachyrhynchus Lock et al. (1992) E. sclateri Lock et al. (1992) Kidney Terra Nova Bay P. adeliae Thls study Syolva station P. adeliae Honda et al. (1986b) Brain Terra Nova Bay P. adeliae This study Syowa station P. adeliae Honda et al (1986b) Testis Terra Nova Bag P. adeliae This study

'Expressed as pg g-' wet wt

Bargagli et al. 1993, de Mora et al. 1993) confirms that Air and snow data, however, suggest that the impact of abiotic matrices in Victoria Land ecosystems have the these emissions is very low. Thus, an explanation for lowest Hg concentrations ever reported. In the study the accumulation of Hg in Terra Nova Bay organisms area, this result was expected as Southern Ocean should be sought among the peculiar physico-chemical waters are substantially isolated from those of other characteristics of this marine environment and adapta- oceans and long-range atmospheric loadings of Hg can tion mechanisms of Antarctic organisms, achieved be excluded on the basis of Hg deposition data (Vandal through a long evolutionary history. et al. 1993). Although the physical and chemical The Ross Sea is a wide embayment of the continen- weathering of rocks in Antarctica is limited by the ice tal shelf between Cape Adare and Cape Colbeck with cover and dry climate, the results of analytical deter- an average depth of 550 m. Water temperature is mination~in surface sediments from Terra Nova Bay always low, ranging from 1°C in summer to -2.0°C in seem to exclude local Hg deposits and by the winter at the surface. Summer availability of the light Italian station. makes and wintering strategies of Regional volcanic emissions are a possible natural primary producers and consumers highly seasonal. source of Hg In the Ross Sea. The significance of vol- Moreover, in the southernmost part of Terra Nova Bay, canic emissions as primary sources of Hg is well docu- a strong katabatic wind determines the recurrence of a mented (Varekamp & Buseck 1986) and the IvlcMurdo coastal polynya (Kurtz & Bromwich 1985) which Volcanic Group along the western margin of the Ross enhances the upwelling of deep nutrient-rich waters Embayment is one of the most extensive alkali volcanic that favour primary production (up to 1119 mgC m-' provinces in the world (Kyle 1990). Besides active vol- d-' in the 0 to 50 m layer; Innamorati et al. 1992).The canoes (Mt. Erebus and Mt. Melbourne), there are phytoplankton blooms twice in summer: once during fumaroles in northern Victoria Land (Bargagli et al. the melt and again during the ice formation; variations 1996a) and recent submarine volcanoes and/or large in underwater irradiance are mainly due to the phyto- intrusive bodies in the western Ross Sea (Kyle 1990). plankton biomass (Innamoratiet al. 1992). 72 Mar Ecol Prog Ser 169: 65-76, 1998

Table 5. Mercury concentrations (pg g-' dry wt) in tissues of an adult Weddell seal from Terra Nova Bay compared with Hg lel~ els in seals from other regions

Region Species n Mean + SD Source

Muscle Terra Nova Bay Leptonychotes weddellii This study Syowa station L. weddellii Yamamoto et al. (1987a) Yamamoto et al. (1987a) Antarctic Peninsula L. weddellii Szefer et al. (1993) Szefer et al. (1993) Lobodon carcinophagus Szefer et al. (1993) Hydrurga leptonyx Szefer et al. (1993) Gulf of St. Lawrence Phoca groenlandica Wagemann et al. (19881 Eastern Australia Arctocephalus pusillus Bacher (1985) Antarctic Peninsula A. gazella de Moreno et al. (1997) Liver Terra Nova Bay L. weddellii This study Syowa station L, weddelLii Yamamoto et al. (1987a) Yamamuiu ei di. (1907aj Antarctic Pen~nsula Szefer et al. (1993) Szefer et al. (1993) Lobodon carcinophagus Szefer et al. (1993)

-Hvdriir-p -1 --- - lqnton,vx Szefer et al. (1993) Eastern Australia A. pusillus Bacher (1985) Antarctic Peninsula A. gazella de Moreno et al. (1997) Alejandro Selkirk Is. A.phllippii Sepulveda et al. (1997) Queen Maud Land Ommatophoca rossi McClurg (1984) Gulf of St. Lawrence P. groenlandica Wagemann et al. (1988) Norway P. groenlandlca Skaare et al. (1994) Skaare et al. (1994) Norway P. vitulina Skaare et al. (1994) Skaare et al. (1994) Norway Halichoerus grypus Skaare et al. (1994) Skaare et al. (1994) Spleen Terra Nova Bay L. weddellii This study Syowa station L. weddellii Yamamoto et al. (1987a) Eastern Australia A. pusillus Bacher (1985) Pancreas Terra Nova Bay L. weddellii This study Syowa station L. weddellii Yamarnoto et al. (1987a) Yamamoto et al. (1987a)

aFemales. "Males. 'Expressed as pg g-' wet wt

As the environmental availability of 1990). In the surface waters of lakes, MeHg is photode- (MeHg), rather than total Hg concentrations, plays an graded at very high annual rates (Sellers et al. 1996) important role in the uptake and transfer of Hg along and the volatilization of elemental Hg from the sea sur- food webs (Fowler et al. 1978, Bernhard & Andreae face is an important component of the global cycle of 1984), the upwelling of waters around the coast of this metal (Amyot et al. 1997).The fact that Terra Nova Terra Nova Bay ma.y be an Important factor for Hg Bay is covered in ice for about 9 mo each year together . The rate of Hg2+methylation is much with the low intensity of solar radiati.on, limited by the higher in deep than in shallow sediments, and h~gh ice and the high density of algae in summer, may sub-thermocline concentrations of MeHg have been therefore enhance the persistence and bioavailability measured in the Pacific Ocean (Mason & Fitzgerald of Hg and MeHg in this coastal environment. Bargag11et al.:Bionl agnification of mercury 7 3

The low temperature of Antarctic water affects the ably the main path of entry of Hg into coastal food metabolic rate of organisms and could reduce the webs. Mason et al. (1996) showed that passive uptake methylation of Hg2+by heterotrophic . of uncharged, lipophilic chloride complexes is the However, demethylation processes are probably also main route of inorganic Hg and MeHg assimilation by reduced. In the same way the cold of the Ross Sea may diatoms and other phytoplankton. MeHg was accumu- decrease the uptake of Hg by marine organisms, but it lated in the cytoplasm of algal cells, whereas inorganic also makes their excretion mechanisms less efficient. Hg was mainly bound to the cell membranes. Conse- According to recent ecotoxicological research (Trudel quently the assimilation of MeHg by zooplankton was & Rasmussen 1997), assimilation of MeHg from food by 4 times more efficient than that of inorganic Hg These fish is 5 to 10 times more efficient than that of inorganic differences in transfer efficiency along the web and in Hg, whereas the elimination of MeHg is 3 times slower excretion efficiency between organic and inorganic and positively correlated with water temperature. fornls of Hg are the main basis for biomagnification of Hg in organisms belonging to long and complex food chains. Biomagnification of mercury in the Terra Nova Bay To evaluate Hg biomagnification processes in coastal food web marine food webs, comprehensive knowledge of the ecology of benthic organisms and their whole-body The results of the present survey show that despite burden of chemical forms of Hg is necessary. Unfortu- the very low concentrations of Hg in marine sediments, nately, the ecology of many Antarctic marine organisms Hg levels in Terra Nova Bay organisms were only is not well known and our data concern total Hg con- slightly lower than or in the same range as those re- centrations. A comprehensive representation of the re- ported for similar species from other parts of the world sults (Fig 3) nevertheless shows a clear increase in Hg (Fowler 1990, Lock et al. 1992, Muir et al. 1992, Sadiq concentrations in the order phytoplankton < herbivo- 1992, Szefer et al. 1993, Joiris et al. 1997, Stewart et al. rous organisms < benthic invertebrates feeding on de- 1997). Although on a fresh weight basis, it is difficult to tritus (either in suspension or deposited) < opportunistic explain the nach lower concentrations llled~ured in scavengers and predators. For molluscs and vertebrate Adelie penguins and Weddell seals from near the species, only concentrations in the digestive gland (or Syowa station (Enderby Land; Honda et al. 1986a, Ya- liver) and muscle were considered. The vertebrate liver mamoto et al. 1987a) and in marine invertebrates from is not homologous and only partly analogous to the in- the Antarctic Peninsula (Yamamoto et al. 1987b, Palmer vertebrate digestive gland, however concentrations of Locarnini & Presley 1995, de Moreno et al. 1997). The 3 Hg in these organs should mainly reflect inorganic coastal areas are very distant and differences in local forms of the metal. In contrast MeHg, which has a bio- factors such as volcanic emissions, water upwelling and logical half-life of years, is accumulated in mollusc and animal ecology (e.g. feeding habits and growth rates) fish muscle mainly as a function of food contamination, could modify the availability and bioaccumulation of species-specific metabolic pathways and age (i.e. expo- Hg. However, some of the low values for Antarctic sure time; Bernhard & Andreae 1984). In muscle of Peninsula marine organisms are rather astonishing be- Trematomus bernacchii from Terra Nova Bay, for in- cause this region has the highest human impact and is stance, up to 96% (medlan 80%) of total Hg is MeHg, also characterized by mineral deposits and volcanic ac- whereas in liver, kidney and gonads this percentage is tivity. Moreover, in a wide survey of Hg in seals, pen- usually <50% (Capelli et al. 1990, Mlnganti et al. 1994). guins and fish from the Antarctic Peninsula Szefer et al. Fig. 3 also shows that although average Hg concentra- (1993) reported values higher than or in the same range tions in the digestive gland of molluscs are in the same as those measured at Terra. Nova Bay. range as or slightly higher than those in liver of midwa- Although Antarctic ocean waters are characterized ter-feeding fish (Cl~ionodracohamatus and Tremato- by short food webs (the krill system), in coastal areas mus hansoni), the Hg content of muscle progressively the biomass of euphausiids may be negligible and the increases from the filter-feeding molluscs (Adamussium webs may have a much more complex structure (Jarre- colbeckj and Laternula elliptica) to the gastropod Teichmann et al. 1997). At Terra Nova Bay the zoo- Neobuccinum eatoni, to fish feeding on amphipods, plankton biomass is rather low (usually a few hundred copepods and euphausiids (T. newnesi, C. hamatus; individuals per m3 of water) and grazers are not food Iwami & Kock 1990) and reaches the highest values in limited; thus the vertical flux of phytoplankton and demersal fish (T hansoni and T. bernacchii) feeding organic detritus from the euphotic zone supports ben- through the year on fish, bivalves and epibenthic crus- thic coinmunities which are very rich in species and taceans (Vacchi et al. 1994, La Mesa et al. 1997). numbers (Gambi et al. 1994). Like in most aquatic Fish and zooplankton play a prominent role in con- ecosystems (Mason et al. 1996) phytoplankton is prob- trolling fluxes of MeHg to Antarctic seabirds and 74 Mar Ecol Prog Ser 169: 65-76, 1998

0 Whole body A Muscle V D~gestivegland or her 1.6 l8 /

Fig. 3. Mercury concentrations in whole organisms and in muscle and liver (or digestive gland) of vertebrates and molluscs from Terra Nova Bay

manne mammals and the results of analytical determi- rous diet consisting of marine organisms, eggs and nations on seabird eggs, feathers and guano agree chicks of penguins and skuas, adult snow petrels and with available information on the ecology of the spe- human refuse from the scientific station (Court et al. cies studied (Young 1994, Kerry et al. 1995). For exam- 1997). ple, concentrations of Hg in eggs, which reflect dietary The quantitative ratio between total Hg concentra- mercury uptake in the period prior to egg-laying tion in liver and muscle of the Weddell seal was much (Monteiro & Furness 1995), were twice as high in eggs higher than in penguins and fish. Pinnipeds have of the (a species migrating north in winter) developed various detoxification mechanisms for Hg, than in eggs of the Adelie penguin (a circumpolar spe- including metallothionein metabolism (Tohyama et al. cies mostly feeding in the Southern Ocean). The south 1986), the formation of selenide granules in the liver polar skua has been seen farther south during summer (Nigro & Leonzio 1996) and excretion of MeHg than any other in the world, but is also known to through the fur (Wenzel et al. 1993). winter (from late June to early October) in the northern Pacific and northern Atlantic (Court et al. 1997). This species can therefore accumulate higher Hg concen- CONCLUSION trations in contaminated environments before laying eggs on the Victoria Land coasts in November. Antarctic manne food webs are usually relatively Hg levels in feathers. reflect those in food eaten simple and short, with krill playing a central role. How- before the moulting period (Fimreite 1979), although ever in coastal environments such as Terra Nova Bay, interspecific differences in moulting and MeHg food webs are much more complex and the fact that Hg demethylation capacity may exist (Lock et al. 1992, was found in a large number of marine organisms Kim et al. 1996). Total Hg concentrations in adult shows that benthic invertebrates are an important link feathers and chick plumage collected at Terra Nova between phytoplankton and fish. Although primary Bay increased in the order snow petrel (mainly feeding producers and consumers had total Hg concentrations on amphipods and copepods) < Adelie penguin (feed- lower than or close to the lower limit of ranges usually ing on zooplankton and fish) < emperor penguin reported for related species from other marine areas, (mostly a fish-feeder) < south polar skua. The high Hg the involvement of benthic organisms in the levels found in the latter are supported by its omnivo- lengthens the chain and causes further biomagnifica- Bargagli et al.: Biom agnification of mercury 75

tion of Hg. There was a sharp increase in Hg concen- in Antarctic ice during the Wisconsin/Holocene transition. trations between benthic molluscs and muscle of de- Nature 323:222-225 mersal fish, fish-eating seabirds and Weddell seals. Capelli R. Minganti V, De Pellegrini R. Fiorentino F (1990) Mercury (total and organic) and selenium in Pagothenia Levels of the metal in tissues of this mammal and eggs bernacchii (Boulenger, 1902) from Terra Nova Bay and feathers of the Antarctic skua were similar to those (Antarctica). Results after two years of research In: reported in samples collected in the northern hemi- Cescon P (ed) Environmental impact in Antarctica. sphere. National Research Council, Rome, p 47-54 Court GS, Davis LS. Focardi S, Bargagli R, Fossi C, Leonzio C, Despite discrepancies with some previous data on Marsili L (1997) Chlorinated hydrocarbons in the tissues of marine organisms from other Antarctic coastal ecosys- south polar skuas (Catharacta maccorrnicki) and Adelie tems, the results of this survey show that Hg concen- penguins (Pygoscelis adeliae) from Ross Sea, Antarctica. trations in the biota of a remote environment, where Environ Pollut 97.295-301 input from local geochemical and man-made sources D'ltri FM (1991) Mercury contamlnation-what we have learned since Minamata. Environ Monit Assess 19: and from long-distance transport is negligible, are not 165-182 necessarily low. As previously found for Cd in marine de Mora SJ, Patterson JE, Bibby DM (1993) Baseline atmos- organisms from the same study area (Bargagli et al. pheric mercury studies at Ross Island, Antarctica. Antarct 1996131, in pristine ecosystems the natural elemental Sc1 5:323-326 de Moreno JEA, Gerpe MS, Moreno VJ, Vodopivez C (1997) composition of organisms may be altered by interac- in Antarctic organisms. Polar B101 17: tions between their ecophysiology and physico-chemi- 131-140 cal characteristics of the environment such as water Denton GRW, Burdon-Jones C (1986) Trace metals in algae temperature, light availability and upwelling of deep from the Great Barrier Reef. Mar Pollut Bull 17:98-106 waters. These interactions should therefore be taken Fimreite N (1979) Accum'ulation and effects of mercury on . In: Nriagu JO (ed)The biogeochemistry of mercury into account when establishing reference areas and/or in the environment. Elsevier/North-Holland Biomedical baseline concentrations of Hg in marine organisms. 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Eciitorjal responsibility: Otto Kinne (Editor), Submitted: Febr~larr*27, 1.9.98; Accepted: AI+. 15, 1998 Oldendorf/Luhe, Germany Proofs received from author(s): July 14, 1998