Transfer of Contaminants in Pelagic Food Chains

In ice-free zones of the Southern Ocean, except in a few areas such as South Georgia, krill is generally absent, and the most common organisms in zooplankton and nekton are herbivorous copepods, salps, small euphausiids, squid and myctophid fish. Antarctic waters lack mid-water crustacean fauna such as Penaeidae which are very common in boreal, temperate and tropical seas. In general, there is scarce knowledge of Antarctic nekton fauna, and very few data are available on their chemical composition. Table 14 reports mean concentrations of trace metals in the liver, kidney and muscle of pelagic myc-tophid fish and two species of octopuses from the Kerguelen Islands (Busta-mante et al. 1998, 2003), and in myctophid fish and cephalopods from the Atlantic Ocean (Schulz-Baldes 1992) and Mediterranean Sea (Miramand and Guary 1980; Fowler 1986). The liver of myctophid fish and the digestive gland of cephalopods are two partly analogous organs which accumulate the highest concentrations of Cd and other trace metals, except Hg. The high Cd content in the liver and kidney (but not the muscle) of G. piabilis indicates that this metal is probably taken in through diet, which mainly consists of very effective Cd accumulators such as hyperiid amphipods and other planktonic crustaceans (see Table 13). Octopus prey includes crustaceans, molluscs and fish. Bustamente et al. (1998) hypothesised that the enhanced accumulation of Cd in Antarctic cephalopods could also be due to the disruption of Cu home-ostatic mechanisms. Cephalopods from the Kerguelen Islands had much higher Cd/Cu ratios and lower Cu contents than samples from other seas. Cd and Cu are known to bind to the same type of metallothioneins in the digestive gland of molluscs. Thus, in marine environments characterised by enhanced Cd bioavailability, it cannot be excluded that this metal can compete and/or substitute Cu in the organ most involved in metal detoxification processes.Very high concentrations of Cd (up to 782 |gg-1 dry wt.) and other metals have also been measured in the digestive gland of cephalopods from the Pacific Ocean (Martin and Flegal 1975).

Data summarised in Table 14 have important ecological implications because cephalopods and myctophid fish occupy predominant niches in food chains of ice-free zones of the Southern Ocean. Although squid are the principal group of cephalopods in the Southern Ocean, data on their elemental composition are not available; as their diet mainly consists of myctophid fish, euphausiids and other crustaceans (Kear 1992), their composition could be quite similar to that of benthic octopuses.

Table 14. Mean trace metal concentrations (|ig g-1 dry wt.) in organs and tissues of myctophid fish and cephalopods from Kerguelen Islands, and related species from the Atlantic Ocean and the Mediterranean Sea

Region

Species

Organ/tissue

Cd

Cu

Hg

Zn

Kerguelen Islands (myctophid fish)a

Gymnoscopelus nicholsi

Liver

4.2±0.3

5.8±1.3

-

93±18

Kidney

2.7±1.0

4.8±1.3

-

86±7

Muscle

<0.1

2.5±0.7

0.21±0.13

9.2±4.0

Gymnoscopelus piabilis

Liver

28±17

10±3

-

142±31

Kidney

16±8

11±5

-

113+23

Muscle

<0.1

1.2±0.4

0.31±0.13

9.9±1.2

Atlantic Ocean (myctophid fish)b

-

Whole

2.0±1.6

7.6±5.6

Mediterranean Sea (myctophid fish)c

Myctophum glaciale

Whole

0.2±0.1

3.6±2.0

0.21±0.2

69±18

Kerguelen Islands (cephalopods)d

Graneledone sp.

Digestive gland

369

1,092

-

102

Whole

39±5

68±30

-

131+19

Benthoctopus thielei

Digestive gland

215

306

-

416

Whole

38±8

68±29

-

166±39

Atlantic Ocean (cephalopods)b

-

Whole

17±8

45 ±21

-

-

Mediterranean Seae

Octopus vulgaris

Digestive gland

50±10

2,500±700

-

1,450±400

Whole

1.2±0.1

260±70

-

150±500

a Bustamante et al. (2003) b Fowler (1986) c Bustamante etal. (1998) d Schulz-Baldes (1992) e Miramand and Guary (1980)

7.3.1 The (Hyper)Accumulation of Cd and Hg in Pelagic Seabirds

Albatrosses and petrels are the predominant flying seabirds in the Southern Ocean (i.e. about 20 species of truly oceanic Procellariiformes, which avoid land except when breeding). Most albatrosses, such as the black-browed (Diomedea melanophris) and light-mantled sooty (Phoebetria palpebrata), prevail in ice-free marine areas whereas petrels (e.g. the southern fulmar, Antarctic cape pigeon and Wilson's storm petrel; Fraser and Ainley 1986) prevail close to the edge of the seasonal pack-ice zone, where krill is the dominant element of the food chain. In ice-free waters, albatrosses (except D. melanophris) and some petrels of the genera Fulmarus, Pterodroma and Pro-cellaria mainly feed on squid and fish (Croxall 1984).

Given their extreme mobility, these seabirds behave as spatial and temporal integrators of persistent contaminants over large areas of the Southern Ocean, and a number of studies (e.g. Anderlini et al. 1972; Norheim 1987; Thompson et al. 1990; Lock et al. 1992; Furness 1993; Hindell et al. 1999; Gonzales-Solfs et al. 2002) show that they accumulate some of the highest Cd and Hg concentrations reported for any vertebrate. As an example, Table 15 reports data from a comprehensive survey performed by Lock et al. (1992) on Cd, Cu, Pb, Zn and Hg concentrations in 64 taxa of tropical, subtropical, sub-Antarctic and Antarctic seabirds. Cadmium concentrations in the kidney are generally two- to fivefold those in the liver. Hindell et al. (1999) measured maximum Cd concentrations (>260 |g g-1 dry wt.) in the kidney of wandering and royal albatrosses, which have predominantly oceanic patterns and are largely confined to the Southern Ocean. Cadmium concentrations in the same range also occur in the kidney of Antarctic petrels and fulmars (Table 15), which feed on krill at the pack-ice edge. Fulmarus glacialoides is slightly larger and only a little paler than its counterpart in the Northern Hemisphere (F. glacialis). Cadmium concentrations in the liver and kidney of northern fulmars from northwest Greenland (Dietz et al. 1996) were lower (21 and 44% respectively) than those in the liver of Antarctic fulmars.

The fact that some species of long-lived albatrosses (e.g. wandering and royal albatrosses may live more than 50 years; Marchant and Higgins 1990) accumulate the same amount of Cd as petrels (mean life expectancy of 15-30 years, depending on species size; Croxall 1984) may be due to differences in diet and in Cd detoxification and elimination capabilities. Cadmium does not generally accumulate with age in seabirds, and concentrations in the liver and kidney of juvenile seabirds are sometimes in the same range or even higher than those in adults (Table 15). This could be due to different foraging or metabolic patterns; in any case, it indicates that seabirds can regulate Cd contents to some extent and that they are able to reduce the Cd load as they get older. As birds cannot eliminate Cd through eggs (e.g. Leonzio and Massi 1989), females and males which adopt similar foraging strategies usually show quite similar Cd concentrations in their organs and tissues.

Table 15. Mean concentrations (|ig g-1 wet wt., ±SD) of Cd in the liver (/) and kidney (k), and of Hg in the liver (/) of adult (a) and juvenile (j) seabirds from the Southern Ocean. (Lock et al. 1992)

Species

Adult/juvenile

Organ

Cd

Hg

Diomedea exulans (wandering albatross)

a

1

14.4±5.3

295±173

a

k

39.4±17.0

Phoebetriapalpebrata (light-mantled sooty albatross)

a

1

9.4±0.1

146±114

a

k

46.5±2.1

j

1

6.1+1.3

9.5±2.9

j

k

21.8±3.2

Thalassoica antarctica (Antarctic petrel)

a

1

21.0

11.1

a

k

43.2

j

1

14.9±2.5

9.2±4.2

j

k

44.2±16.4

Fulmarus glacialoides (Antarctic fulmar)

j

1

18.7±6.9

19.9±7.9

j

k

43.1±18.8

Daption capense (cape pigeon)

a

1

9.3±5.8

14.5±12.6

a

k

32.8±9.4

The behaviour of mercury is completely different from that of cadmium. Mercury, in particular methylmercury (MeHg), is biomagnified in aquatic food chains; its bioaccumulation is more similar to that of hydrophobic organic pollutants than to that of other metals (Bargagli 2001). All animals can generally eliminate inorganic Hg in several weeks, whereas the biological half-life of MeHg is months or years. Methylmercury therefore progressively accumulates in muscle and other tissues, reaching peak concentrations in long-lived animals at higher levels of the food web. The proportion of Hg and MeHg varies in different tissues and organs depending on the trophic status, age, and species-specific adaptive capacity for detoxification and elimination of the metal. Methylmercury concentrations in seabirds are usually much higher than in birds of terrestrial ecosystems because the former feed on crustaceans, fish and squid which "preconcentrate" MeHg by eating phyto-and zooplankton organisms. The highest concentrations of total Hg reported for seabirds and marine vertebrates throughout the world oceans probably occur in Procellariiformes (albatrosses and petrels) from the Southern Ocean. Hindell et al. (1999) measured 1,800 |gg-1 dry wt.(or 680 |gg-1 wet wt.) of Hg in the liver of a wandering albatross, and data in Table 15 show that although the Hg body burden increases with age, even in juvenile Antarctic seabirds average Hg concentrations are always >9 |g g1 wet wt. This huge bioaccumulation is rather surprising.

As mentioned in the preceding chapter, although concentrations of Hg and MeHg in Southern Ocean waters are unknown,values are probably rather low. Low concentrations have also been reported for sediments, phytoplankton, macroalgae and zooplankton from the Ross Sea (Bargagli et al. 1998a), and concentrations in Antarctic krill are always <0.1 |g g1 dry wt. (Fig.45). As discussed by Hindell et al. (1999) and Bargagli et al. (2000), the bioaccumulation of Hg in Antarctic seabirds is a natural process mainly determined by species-specific life histories. Larger and long-lived species such as wandering albatrosses or grey petrels, which largely feed on squid, fish or carrion (Lock et al. 1992), have the highest Hg burden. Since wandering albatrosses have a low reproductive rate (one egg every 2 years) and replace feathers over a period of years rather than annually, they have very few ways of eliminating MeHg. Moulting is an important route for MeHg excretion, because seabirds deposit MeHg in their feathers during growth (Fimreite 1979). Part of the MeHg ingested with food is demethylated in the liver, where it is stored as inorganic molecules (Thompson and Furness 1989). In three species of albatrosses and a grey petrel, for instance, MeHg concentrations in the liver ranged from 4.8 to 16 |g g1 wet wt., and inorganic Hg concentrations reached 280 |g g1 wet wt. (Lock et al. 1992). Despite efficient demethylation mechanisms, levels of MeHg and inorganic Hg in the liver of Antarctic seabirds are higher than those usually found to be toxic for terrestrial and freshwater birds (Sheuham-mer 1988); it has therefore been hypothesised that the latter are more sensitive than some Procellariiformes to Hg.

In addition to inorganic Hg, albatrosses and petrels also accumulate Se in the liver and kidney. Kim et al. (1966) measured a maximum value of 113 |g g-1 dry wt. in the liver of black-footed albatrosses. Ohlendorf et al. (1988) reported high incidences of bird embryo and adult mortality due to the toxic effect of Se. However, small quantities of this element are essential to the metabolism of birds and mammals, and there is evidence that Se acts as an antidote to the toxic effects of some heavy metals, particularly Hg (Koeman et al. 1973). Although Hg detoxification mechanisms in seabirds are not well known, co-accumulation of Hg and Se in the liver probably derives from the formation of inorganic Hg-Se complexes. Kim et al. (1996) found an equivalent molar ratio of 1:1 between total Hg and Se concentrations in grey petrel and light-mantled sooty albatrosses, which accumulated more than 100 |g g-1 dry wt. of Hg in the liver. On the contrary, this relationship did not emerge clearly in individuals with relatively low levels of Hg, and fluctuating molar ratios were ascribed to a different degree of exposure to Hg, species-specific demethylation capacity, and elimination through moulting. Dietz et al. (2000) reported a surplus of Se with respect to Hg (on a molar basis) in various tissues of Arctic seabirds and suggested that excess Se may reduce the potential threat of Hg poisoning.

In spite of the bioaccumulation of potentially toxic metals, populations of wandering albatrosses at South Georgia and in other sub-Antarctic areas are declining mainly because they are caught on hooks set by vessels which tow huge, heavily baited long-lines for Patagonian toothfish and other fish species. Seabird carcasses have sometimes been frozen to study their chemical composition. However, less destructive biomonitoring approaches such as the analysis of feathers can be used to evaluate interspecies and geographic variations in Hg bioavailability. In agreement with data on the liver and kidney, Fig. 46 shows that average Hg concentrations in feathers from Antarctic albatrosses and southern giant petrels (Thompson et al. 1993) are higher than those in feathers from seabirds at Foula Island (Shetland; northern Atlantic; Thompson and Furness 1989). By analysing museum feather samples of various species of seabirds from southwest Britain and Ireland, Thompson et al. (1992) found that anthropogenic emissions caused a threefold increase in Northern Hemisphere Hg concentrations over a 100-year period. On the contrary, the feathers of Southern Hemisphere Procellari-iformes collected before and after the 1950s revealed no significant increase in Hg concentrations. These results led Thompson et al. (1993) to conclude that the bioaccumulation of Hg in albatrosses and petrels is mainly due to natural processes.

A number of papers have been published on POP concentrations in pelagic seabirds. However, these studies analysed eggs and different organs or tissues, and adopted different measurement units. Available data are highly variable, and it is difficult to interpret spatio-temporal variations in POP concentrations within Antarctic seabirds due to differences in trophic levels and to the wide

Fig. 46. Average concentrations (|g g-1, ±SD) of total Hg in feathers of seabirds from South Georgia (Thompson et al. 1993) and Foula (Shetland Is.; Thompson and Furness 1989)

I.Il

Southern Ocean

North Atlantic

I.Il dispersion of some species outside the breeding area. Conroy and French (1974) found that pp'-DDE in the liver of giant petrels collected on Signy Island in 1968-1969 ranged from 20 ng g-1 wet wt. in younger birds to 30 ng g-1 wet wt. in 5-15 year old birds. Monod et al. (1992) detected DDE and PCBs in all seabirds sampled on the Kerguelen Islands in 1971 and 1975, but DDT and DDD were present only in penguins and albatrosses. Gardner (1983) measured high concentrations of chlorinated hydrocarbons in fat-storage tissues of feral cats on Marion Island (feeding mainly on seabirds). Gardner et al. (1985) subsequently measured concentrations of DDT, DDE, PCBs and dieldrin in eggs from 24 species of seabirds breeding on Marion and Gough islands. Relatively higher concentrations (expressed as ng g-1 of whole egg) were measured in eggs of wandering albatrosses and southern giant petrels: DDE values ranged from 56 to 4,242, DDT from 5 to 122,PCBs from 13 to 211, and dieldrin from 1 to 3. Eggs collected after the 1980s generally contained higher PCB levels than those of the same species collected in earlier periods. Luke et al. (1989) provided a comprehensive review of DDT residues in eggs of Antarctic seabirds, and measured the highest levels in species which breed in Antarctica and then migrate to regions well north of the Antarctic Convergence. Concentrations of HCB, DDE and PCB in the eggs of northern giant petrels were 0.11,0.95 and 1.8 |g g-1 wet wt. respectively. There was an apparently consistent increase in p,p'-DDE concentrations in eggs of southern and northern giant petrels collected in the period 1978-1983. Van den Brink (1997) determined PCB and HCB concentrations in preen oil from birds with different distribution ranges - those restricted to Antarctica and the Southern Ocean year round (e.g. snow petrels, Antarctic petrels, southern fulmars and Adelie penguins), those which spend summers in Antarctica and winters in sub-Antarctic regions (cape petrels) and, finally, a seabird (the common tern) of the Northern Hemisphere which spends summers in temperate regions and winters in subtropical regions. The first group of birds had low total PCB contents (mean=270 ng g-1 fat) and rather high HCB concentrations (mean=497 ng g-1 fat). PCB concentrations were significantly higher in cape petrels (mean=1,207 ng g-1 fat) than in birds restricted to the Southern Ocean. Cape petrels also showed the highest HCB concentrations (mean=2,096 ng g-1 fat). In the common tern, PCB concentrations were much higher (mean=13,095 ng g-1 fat) and HCB concentrations were much lower (mean=3 ng g-1 fat) than those in Antarctic seabirds.As HCB is relatively volatile,has a long environmental half-life and accumulates in species at higher trophic levels (Mackay et al. 1992),the much higher HCB content in Antarctic seabirds than in common terns from the Northern Hemisphere was attributed to the global distillation process. Based on HCB levels, seabirds from sub-Antarctic regions were considered at risk from the possible toxic effects of POPs.

In Antarctic seabirds the potential risk from exposure to POPs may be enhanced by the extreme variability of physiological conditions throughout the breeding season. During periods of starvation, the fat pool of birds decreases, and concentrations of POPs stored in fat consequently increase (Subramanian et al. 1986). To investigate the effects of breeding ecology on concentrations of organochlorines, van den Brink et al. (1998) collected blood and uropygial oil samples from southern fulmars. They found that fluctuations in HCB and p,p'-DDE concentrations were related to changes in body mass, while PCB and dieldrin contents did not vary significantly during the season. It was therefore hypothesised that the two groups of compounds were stored in different tissues, and that utilisation of stores in these different tissues at different moments of the breeding cycle could produce fluctuations in the content of various POPs during the season.

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