Antarctic: Persistent Organic Pollutants and Environmental Health in the Region

Antarctic: Persistent Organic Pollutants and Environmental Health in the Region S Corsolini, University of Siena, Siena, Italy & 2011 Elsevier B.V. All rights reserved.

Abbreviations AhR CB CFC CHLs DDT p,p0 -DDE EDs HCB HCHs IARC OCP PBDE PCBs PCDD PCDD POP TEF TEQ WHO

aryl hydrocarbon receptor carbamate chlorofluorocarbon chlordanes dichloro diphenyl trichloroethane p,p0 -dichlorodiphenyltrichloroethane endocrine disruptors hexachlorobenzene hexachlorocyclohexans International Agency for Research on Cancer organochlorine pesticide polybrominated diphenyl ether polychlorinated biphenyls polychlorinated dibenzofuran polychlorinated dibenzodioxin persistent organic pollutant toxic equivalency factors toxic equivalents World Health Organization

Glossary Common name Scientific name Aldrin Ade´lie penguin Pygoscelis adeliae Antarctic krill Euphausia superba Antarctic naked dragonfish Gymnodraco acuticeps Antarctic scallop Adamussium colbecki Antarctic skua Catharacta antarctica Antarctic whelk Neobuccinum eatoni Blackfin icefish Chaenocephalus aceratus Copepod Centropages hamatus Chlordanes (CHLs) Dieldrin Eldrin Endrin Elephant seal Mirounga leonina Emerald rockcod Trematomus bernacchii Emperor penguin Aptenodytes forsteri Humped rockcod Gobionotothen gibberifrons

Heptachlor Leopard seal Hydrurga leptonyx Mackerel icefish Champsocephalus gunnnari Mirex Silverfish Pleuragramma antarcticum Snow petrel Pagodroma nivea South Polar skua Catharacta maccormicki Toxaphenes Weddell seal Leptonychotes weddellii

Introduction Ecosystems and Contamination in Antarctica Antarctica is a snow-covered continent surrounded by the Southern Ocean that isolates it from other land masses (Figure 1). The Antarctic Circumpolar Current (ACC) is a physicochemical boundary that isolates the Southern Ocean from the other oceans. The geographic isolation and extreme climate of Antarctica and the Southern Ocean are responsible for both their late discovery by man and the absence of any human impact (towns, industry, and mining), except for the scientific stations. Unfortunately, many studies have demonstrated that even this remote continent and ocean has been reached by contaminants such as persistent organic pollutants (POPs). Contamination in the Antarctic ecosystems was first reported in 1966, and, since then, there has been an increasing interest in studying and monitoring the presence of pollutants in this pristine region of the world. This awareness has been growing during the recent years, when the Arctic has been reported as a final sink for POPs. The ACC isolates the Southern Ocean from any oceanic inputs, which, as a consequence, is evaluated to be very low. The North Atlantic Deep Water (NADW) is approximately 2 km in depth and flows southward; its path can ultimately be traced into the Southern Ocean as it mixes with the ACC. It brings waters from the Northern Hemisphere, where POPs are largely used. Some researchers think that the NADW brings contaminants from the boreal hemisphere that have been used at least a couple of years earlier. Migratory animals (South Polar skuas (Catharacta maccormicki), other seabirds, and whales) may be a minor source of pollutants in polar regions because of their excrements and carcasses.

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Antarctic: Persistent Organic Pollutants and Environmental Health in the Region

W

The presence of synthetic and toxic chemicals in the Antarctic ecosystems is partially associated with the activities of the scientific stations; nevertheless, the main source of pollutants for this remote continent is the atmospheric transport. Volatile or semivolatile contaminants may be transported to the remote Antarctic continent mainly by air mass. Cold condensation and global fractionation have been proposed as mechanisms whereby POPs can reach polar regions; both POP condensation and fall out depend on physicochemical properties of the molecules and air temperature (Figure 2). Owing to the extreme cold climate and winter darkness, the degradation of deposited POP is very slow in the polar regions and they may be entrapped in the ice. Through ice melting, POPs are released again into the ocean, where they enter the food webs (Figure 3), bioaccumulate in the tissues of organisms, and biomagnify. Antarctic trophic webs are relatively simple and brief: animals at the top of the food webs depend on few key species such as silverfish (Pleuragramma antarcticum) and krill (Euphausia superba) that are the prime food source for several bird species and marine mammals, which depend on them either directly or indirectly (Figure 4). Hence, the decline in the population of stock of key

ar m e a po mis nd te ra sio m tio n > n ar pera de eas te po sit ion

Map of Antarctica and the Southern Ocean.

va

Figure 1

(e

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POPs

Cold climates of polar regions (deposition > evaporation)

High volatility (CFCs)

Figure 2

T) (DD tility a l vo ty Low latili e vo Ns) t a i d C rme s, P Inte , PCB B C (H

The long-range transport of POPs (schematic).

species can have devastating impacts on the marine ecosystem. Owing to the differences in geographical features and ecosystem characteristics, organisms inhabiting

Antarctic: Persistent Organic Pollutants and Environmental Health in the Region

85

(a)

POPs

2

POPs

POPs

1 Trophic web 3

(b)

POP

Deposition

Winter: ice entrap xenobiotics

Summer: xenobiotics released into seawater enter trophic webs

Figure 3 The relationship between abiotic and biotic distribution of POPs (a), and the release of POPs to seawater during summer ice melting (b).

Top predators

Other cetaceans Predators

Killer whale

Pollutants Leopard seal

Squid Flying seabirds Penguins Seal Other fish

Silverfish Herbivores Primary production

Figure 4

Zooplankton: krill, copepods, amphipods, fish larvae, etc. Phytoplankton

Outline of an Antarctic trophic web.

Antarctica are exposed to different levels and patterns of organochlorine compounds; the evaluation of contaminant concentrations in their tissues provides information on the extent of contamination in these remote areas of the globe. Furthermore, because marine species living in the polar regions have greater lipid content than temperate or tropical species, they are susceptible to accumulating high concentrations of persistent, toxic, and lipophylic contaminants.

POPs include several groups of chemicals (Figure 5) with similar structures and physical–chemical properties that elicit similar toxic effects. They have been used extensively worldwide in agriculture (pesticides, e.g.: aldrin, chlordanes, DDT, dieldrin, endrin, HCB, mirex, heptachlor, toxaphenes), industrial (PCBs, PBDEs) and health (dichloro diphenyl trichloroethane (DDT)) applications. All these chemicals are synthetic, ubiquitous and hydrophobic and show long-range transport potency. They are persistent in soils and sediments, with environmental half-lives ranging from years to several decades or more. They are not very volatile and show high chemical and thermal stability and low biodegradability. Because of their resistance to biodegradation, they are also called xenobiotics. These chemicals bioaccumulate in the lipid components of tissues in organisms and accumulate in organisms through food webs. Consequently, the principal route for chronic exposure of both animals and humans is through diet. Mounting evidence suggests that populations of various animal species are, or have been, adversely affected by exposure to POPs. Some xenobiotics mimic

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Antarctic: Persistent Organic Pollutants and Environmental Health in the Region Cl

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Aldrin C10H6Cl8

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Chlordanes (CHLs) C12H8Cl6

Dieldrin C12H8Cl6O

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p,p′-dichlorodiphenyltrichloroethane (p,p′-DDE)

Eldrin

C14H9Cl5

C27H30O16

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Hexachlorobenzene (HCB) C6Cl6

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Endrin C12H8Cl6O

Heptachlor C10H5Cl7

Mirex C10Cl12

ortho Cln

X

meta CH3

X 3

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X Polychlorinated dibenzofurans (PCDFs)

Polychlorinated biphenyls (PCBs) C12HxCly

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Polybrominated diphenyl ethers (PBDEs)

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Persistent organic pollutants.

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Toxaphenes

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Polychlorinated dibenzodioxins (PCDDs) C12H4Cl4O2

Antarctic: Persistent Organic Pollutants and Environmental Health in the Region Normal

Cl

Endogenous endogenous hormone hormone (EH) (EH)

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EH Cl

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Receptor (R) (R) Receptor action action Cell cell

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ED R Cell cell

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Action

ED R Cell cell

Cl 33′44′55′ (PCB169)

Action

Figure 6 Schematic mechanism of action of the endocrine disruption [it shows the competition between the endogenous hormone (EH) and the endocrine disruptor chemical (ED) for the receptor (R) that is the first step of the mechanism. The resulting ‘‘action’’ in normal conditions (EH-R complex) can be reduced or amplified in relations to the agonistic or antagonistic role of the ED].

natural hormones and are defined as xenoestrogens, namely, environmental chemicals that act as estrogens. Effects on the functioning of the endocrine system are the first damages to be detected. In fact, some POPs are known as endocrine disrupter compounds (EDCs), meaning that they are able to interfere with functions of the endocrine system (Figure 6), although not all POPs are EDCs. It has been suggested that only those that cause adverse effects on individual organisms through primary effects on endocrine systems that could lead to population- and community-level impacts are EDCs. They include the following most widespread and well-known classes of contaminants: polychlorinatedbiphenyls (PCBs), polychlorinated-dioxins (PCDDs), polychlorinated-furans (PCDFs), polychlorinated-diphenyl ethers (PBDEs), polychlorinated-biphenyls (PBBs), perfluorinated compounds (PFCs), and other halogenated hydrocarbons, often used as a pesticides. The most toxic POPs are the PCDDs and the PCDFs. They are structurally similar chlorinated hydrocarbons, produced as a by-product in many technical mixtures of halogenated compounds, including pesticides, and during paper and pulp bleaching. They also occur through urban and industrial waste incineration, metal production, fossil fuel and wood combustion, and are still present in PCB-filled electrical transformers. 2,3,7,8-Tetrachlorodibenzo-p-dioxin (2,3,7,8-TCDD or TCDD) is known to be the most toxic compound for organisms. The International Agency for Research on Cancer (IARC) announced in 1997 that the most potent dioxin, the 2,3,7,8-TCDD, is considered a Class 1 carcinogen, meaning a known human carcinogen, and it has

Cl

2

8 Cly

Clx 3

7

Figure 7 Chemical structure of 2,3,7,8-TCDD, PCB169, and rotation of the C–C bond of the biphenyl that allows the chemical planar configuration of a dioxin-like PCB.

been confirmed by the Environmental Protection Agency (EPA). TCDD binds to the cytosolic aryl hydrocarbon receptor (AhR) to build a substrate–receptor complex that can enter the cell nucleus and interfere with the expression of some genes. This interaction contributes to an increase in or induction of 2,3,7,8-TCDD inducible genes such as CYP1A1. There is a decrease in receptor binding affinities as the lateral substitutions decrease. Toxic effects due to POPs include cancer, reproductive, and developmental problems (e.g., low birth weight, hormone alterations, lower IQ , and emotional problems), alterations of the immune system, such as decreased ability to fight cancer and infections, endocrine disruption (affecting the thyroid and sex hormones), central nervous system defects, effects on the nervous system, liver damage, skin and eye disease, and death. Apart from TCDD, many other chemicals elicit the same toxic effects due to isostereoisomerism with TCDD. Many POPs act in the same way as TCDD and are known as dioxinlike compounds; these include all the PCDDs and PCDFs that have chlorine atoms in the 2,3,7,8 positions on the molecule, plus certain specific PCBs and other compounds that can be isostereoisomers of TCDD (Figure 7) and show AhR-mediated responses in cells.

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Antarctic: Persistent Organic Pollutants and Environmental Health in the Region

Toxic equivalency factors (TEFs) express the toxic potency of a chemical in relation to that of the TCDD and can be used to calculate 2,3,7,8-TCDD toxic equivalents (TEQs), which are an important tool for estimating risk in organisms. The methods are based on the fact that dioxins cause AhR-mediated effects and that exposure is typically due to mixtures of dioxins. TEF values are based on in vitro and in vivo induction potency of the AhR; TCDD TEF was assigned a value of one and consequently all the other chemicals have a TEF lower than one. The total toxicity can be calculated as follows: TEQ s ¼

X X ½PCDDi  TEFi  þ ½PCDFi  TEFi  n1

þ

X ½PCBi  TEFi 

n2

n3

where PCDDi, PCDFi, and PCBi are the concentration of each congener, the specific TEF value of each P TEF Pi is P congener, and n1 , n2 , n3 are the sums of the TEQ values of each class of contaminants. Because polar organisms have developed few methods to deal with foreign substances, evaluating levels and potential toxicity in Antarctic species is an important means to understanding the biological impacts in those organisms whose detoxifying enzyme systems are not yet fully understood. Hundreds of thousands of different industrial chemicals are or have been produced worldwide, but only a few of them were studied in Antarctic organisms; many of these chemicals are listed or are under consideration of the Stockholm Convention. They are pesticides (aldrin, chlordanes (CHLs), DDT, dieldrin, endrin, heptachlor, mirex, and toxaphene); industrial chemicals (PCBs, hexachlorobenzene (HCB), also used as pesticide); unintentional by-products (most important for their toxic potential are PCDDs and PCDFs) (Figure 5); in addition, the study of the so-called emergent POPs in Antarctic ecosystems is also crucial because of their increasing contamination at the high latitudes of the Northern Hemisphere. These chemicals are the PBDEs used worldwide as flame retardants (Figure 5). Most volatile chemicals, such as HCB and low-halogenated PCBs and PBDEs, are expected to reach the polar regions faster than less volatile ones, such as the highly halogenated pesticides (OCPs), PCBs or PBDEs. Unlike migratory species that reach Antarctica in summer for feeding (e.g., cetaceans), or reproduction (e.g., seabirds), those endemic species of the Antarctica can give exact indications on the contamination levels in this remote and still pristine continent. The area characterized by polar or subpolar conditions is delimited by the Antarctic Convergence (northern boundary of the ACC), including the sub-Antarctic islands (Figure 1). Among POPs, the most studied in Antarctic organisms are PCBs 4DDTs 4HCB. It is important to clarify that

Antarctic biota refers mostly to marine organisms; the terrestrial species of flora and fauna are very few (as expected in a cold desert): lichens, moss, and small invertebrates; no large plants and animals can be found in the Antarctic continent. A couple of species of plant (Deschampsia antarctica and Colobanthus quitensis) grow up in the Antarctic Peninsula. The terrestrial vegetation and fauna as well as most of the small and large marine animals show a very slow growth and often are very longlived, in relation to the extreme environment. Moreover, the feeding period is often concentrated during the summer months, when the climate allows the plankton to bloom, and all the species of the trophic webs have food and better conditions to breed.

Health of Antarctic Organism Environmental health is usually correlated to human health and it calls to mind human well-being. Following the World Health Organization definition, it addresses all the physical, chemical, and biological factors external to a person and all the related factors impacting behaviors. It encompasses the assessment and control of those environmental factors that can potentially affect health. It is targeted toward preventing disease and creating healthsupportive environments. Essentially, human health cannot be regardless of environmental health. Humans are only occasional inhabitants of Antarctica for scientific purposes, and their presence and all activities are regulated by the Antarctic Treaty; the same treaty also controls tourism, and tourists cannot disembark without the permission and the guide of authorized scouts. In the light of these considerations, it is very important to study the environmental health in Antarctica: this continent is considered to be crucial for the ecological equilibrium of the planet, with regard, for instance, to the global climate, the freshwater mass balance, the global ecosystem equilibrium, and health. The Antarctic ecosystems are very fragile, and even a very small alteration can cause a dramatic consequence, often irreversible; their resilience capacity is very low. The knowledge of the environmental levels and patterns of toxic persistent contaminants can improve the knowledge on the related risk for organisms, including humans, and it is very important both for an evaluation of the global environmental health and for other possible consequences at a global scale. Levels and Patterns of Contaminants Among xenobiotics, PCBs may be considered the most known, widely distributed, and studied. The accumulation of PCB congeners and isomers, their patterns, and relative abundance may give important information on their global transport, bioaccumulation paths, and distribution in organisms. The profile of PCB contamination

Antarctic: Persistent Organic Pollutants and Environmental Health in the Region Tri-CBs

Tetra-CBs

Penta-CBs

Hexa-CBs

Hepta-CBs

Octa-CBs

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Nona-CBs

Algae Yoldia Whelk Scallop Sea urchin Sea star Sea cucumber Rockcod_m Rockcod_l 0%

20%

40%

60%

80%

100%

Figure 8 Class of isomer composition of PCBs in some species of Antarctic benthic organisms (Rockcod_m = rockcod muscle, Rockcod_l = rockcod liver).

in Antarctic organisms is often different from that of other parts of the world. In fact, lower chlorinated congeners often show high concentrations with respect to higher chlorinated ones. Tri- to penta-CBs were 35–65% of the total PCB residue in a benthic trophic chain of the Ross Sea (Figure 8). In these organisms, fingerprints confirm different patterns between species, likely depending on specific metabolisms, sex, age, and breeding activity. Fish and invertebrates show low detoxifying activity to metabolize PCB138, 153, and 180; their concentrations are lower in the prey with respect to their predator (sea urchin, Antarctic scallop (Adamussium colbecki), Antarctic whelk (Neobuccinum eatoni)oemerald rockcod (Trematomus bernacchii); Antarctic scalloposea star; Antarctic scalloposea urchin; algaeosea urchin; sea urchin, Antarctic scalloposea star) (Figure 9). By comparing fingerprints of Antarctic seawater and organisms, some important differences emerge. Lower chlorinated PCBs show remarkable concentrations in seawater, whereas high chlorinated ones are absent. Penta- to octacarbamate (CB) congeners are detectable only in organisms where they make up most of the residue. Fish show remarkable levels of low-chlorinated congeners as they assume them from water and food; in fact, lowchlorinated PCBs, being slightly biodegradable, can reach a rapid equilibrium between seawater and fish. In general, the fingerprints of emerald rockcod and Centropages hamatus, compared to those of Ade´lie penguin (Pygoscelis adeliae) and Weddell seal (Leptonychotes weddellii), emphasize a possible excretion of lower chlorinated congeners in fish; penguin and seal accumulate contaminants mainly from food, and therefore show different congener compositions, with most of the residue being made up by hexa- and hepta-CBs.

Only a few scientific articles have reported data on the POP presence in terrestrial organisms. An interesting study published in 1991 reported the detection of HCB, HCHs, DDTs, and PCBs in moss and lichens from Kay Island, Ross Sea. Levels were lower than those detected in similar species from Northern Europe at that time. Interestingly, alpha-HCH level was higher than gammaHCH level (0.17 and 0.04 ng/g dry wt, respectively), indicating the arrival of ‘‘old’’ air; this pattern is typical of remote regions that currently reflect past usage of alphaHCH enriched technical mixtures, while gamma-HCH is at present found in areas under higher anthropogenic impact, due to its presence in mixtures of current use. The trend in moss ... and lichen samples from the Antarctic Peninsula was gamma-HCH 4alpha-HCH (0.71 and 0.32 ng g1 dry wt, respectively). This pattern is due to the transport of HCHs from areas where they were still used at the time of sampling, and it is typical of most of the anthropized regions. HCB was detected in lichen and moss from both the Antarctic Peninsula (0.49 ng g1 dry wt) and the Kay Island (0.3 ng g1 dry wt), as well as p,p0 -DDE and p,p0 -DDT. The DDE/DDT ratio was 0.7 in both locations, indicating a distance from the application sites, but a likely continuing input from distant sources at the time of sampling. PCBs were below detection limits in Kay Island samples (o5 ng g1 dry wt) and were 9.9 ng g1 dry wt in the Antarctic Peninsula samples. The POP concentrations in organisms of the lower levels of the trophic webs (plankton, krill, and invertebrates) are inhomogeneous and at different levels of magnitudes. Concentrations do not increase from one trophic level to the next or from the smaller to the larger organisms, as expected. This may be due to various reasons: first of all, different time of sampling can play an

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Antarctic: Persistent Organic Pollutants and Environmental Health in the Region

Trematomus bernacchii (benthic feeder) 14.5 ? Neobeuccinum eatoni (necrophagous) 0.793

Odnotaster validus (omnivorous, filter feeding) 5.82

Yoldig eightsi (deposit feeder on mud, filter feeding) 0.704

Atamusium colbecki (filter feeding, detritivorous) 0.989

Holoturians (filter feeding or detritivorous) 8.179

? Sterechinus neumayeri (herbivorous) 6.478

I. cordata 1.351

Figure 9

PCB concentrations (ng g1 wet wt) in relation to the position of organisms in the trophic web (schematic).

important role in the bioaccumulation. Ice melting is reported as one of the major causes of contamination in polar regions as contaminants trapped in the ice can be released in the seawater during summer. Thus, organisms living under the pack ice (krill, small larvae, and other planktonic organisms) accumulate POPs the first, and the POP transfer from seawater to organisms may depend on metabolism rate, temperature and POP physicochemical and accumulation properties. Because ice melting occurs at different times in different sites, levels detected in planktonic organisms may vary a lot depending on the time of collection. Second, the surface of small planktonic organisms can adsorb particulate organic material containing contaminants deriving from ice melting, and this could explain the variability of concentrations, depending on their different ratio surface/volume. It seems that no biomagnification occurred between plankton and krill. It is likely that plankton accumulates contaminants mainly through bioconcentration and adsorption, whereas diet may be a minor intake path. The assessment of the bioconcentration factor (BCF) in a pelagic trophic web (phyto-, zooplankton, krill, silverfish, and Ade´lie penguin) of the Ross Sea showed that the largest increment in PCB concentration was from water to phytoplankton, and from fish to seabirds. The progressive amplification of the quantity of contaminants in the organisms is due to bioconcentration and biomagnification; bioconcentration can prevail at the lower levels of the trophic webs, whereas biomagnification can become the main route of contamination at the higher ones, where the feeding habit of a predator plays a crucial role in POP uptake. The presence of HCH isomers was investigated in seawater and krill samples collected in the Ross Sea, at

the margin of pack ice, where melting occurs. Concentrations of HCHs ranged 0.049–0.322 ng g1 wet weight (wet wt) in krill and 0.65–1.53 pg l1 in seawater, with a predominance of gamma-HCH in all krill and seawater samples. Heptachlor, heptachlor epoxide, dieldrin, and aldrin have also been detected in Antarctic low trophic level organisms. These pesticides are present in the Antarctic environments, but the paucity of data does not allow any speculation on bioaccumulation mechanisms and patterns. Among the Antarctic mollusks and benthic invertebrates, the Antarctic whelk showed slightly lower concentrations than its prey, the Antarctic scallop. The scallop is a filter feeding, and feeding habits may be responsible for bioaccumulation; in fact, a filter-feeding organism accumulates more POPs than expected in relation to its trophic position in the food web. Moreover, many Antarctic organisms (e.g., the sea star) accumulate lipids during the breeding season and to overwinter; as a consequence, it may pose a major risk for them to accumulate POPs compared to organisms that accumulate glycogen to overwinter. A decreasing trend of PCB levels might be hypothesized between samples collected at the end of the 1980s and the beginning of the 1990s, and those collected in 2000. CHLs have been largely used as insecticides in the Southern Hemisphere. As they are persistent and show long-range transport, they can reach the Antarctica and enter the trophic webs. All CHL compounds were below the detection limits in krill from the Ross Sea samples, whereas nonachlor and trans-CHL were detectable in samples from the Weddell seal, where mirex was also detected. A possible difference in the CHL

Antarctic: Persistent Organic Pollutants and Environmental Health in the Region

contamination between the Ross Sea and the Weddell Sea may be due to the vicinity of the Weddell Sea to the South American lands. Pentachlorobenzene (QCB), PBDEs, polychloronaphthalenes (PCNs), non-ortho PCB congeners, PCDDs, and PCDFs were also detected in krill samples collected in the Ross Sea, confirming the presence of a wide variety of POPs in the Southern Ocean and their accumulation even at the lower levels of the pelagic and benthic trophic webs. There are only few species of Antarctic fish that are fished for commercial use; krill and the Antarctic toothfish are caught by trawls and they are used both for human consumptions and for other purposes (animal diets); fishing in Antarctica is regulated by the Antarctic Treaty. The demand for fishing in Antarctic seawaters is increasing recently because fish stocks of other oceans are decreasing. Hence, it is important to know the contaminant levels and the health status of stocks in these species. The Antarctic toothfish (a long-lived large fish heavily fished for human consumption) showed higher concentration of PCBs, DDTs, and HCB with respect to other species like Antarctic naked dragonfish (Gymnodraco acuticeps), and the emerald rockcod sampled during the 1987–90 seasons in the Ross Sea (741 S, 1641 E), likely in relation to its large size that allows bioaccumulation with age. The relative abundance of HCB, DDT, and PCBs in some fish species from the Ross Sea and the Weddell Sea differed: it was HCB4DDTs4PCBs in humped rockcod (Gobionotothen gibberifrons), mackerel icefish (Champsocephalus gunnari), and blackfin icefish (Chaenocephalus aceratus) from the Weddell Sea, and PCB4DDT4HCB in those species from the Ross Sea. Many samples showed the following pattern: HCB4p,p0 -DDE, which is different from organisms from other locations of the world. DDE has a higher bioconcentration potential (log BCF ¼ 4.7 in fish) compared to the HCB (log BCF ¼ 3.1– 4.5 in fish), but it is volatile and easily transported by air masses (HCB and p,p0 -DDE vapor pressure are 1.8  106 and 1.7  108 atm, respectively). Therefore, fish-eating predators may accumulate a greater amount of HCB than p,p0 -DDE, which might be less available to organisms in cold polar region. A similar phenomenon has already been described for HCHs, with higher concentration in the Northern Hemisphere. The global transport is responsible for this pattern: due to global fractionation, highly volatile POPs (e.g., HCB) reach the polar regions quite rapidly compared to heavier molecules. Ice can be a trap for those chemicals such as HCHs and HCB, and can release them during melting as well as PCBs. Fish from the Antarctic Peninsula and from the Ross Sea, seabirds, and krill showed a HCB4p,p0 -DDE pattern. On the contrary, seals seem to accumulate more DDE than HCB as reported for Weddell seal from the Ross Sea, and

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for Weddell seal and elephant seal (Mirounga leonina) from the Antarctic Peninsula. DDT and PCB concentrations showed a decreasing time trend in the silverfish collected in the Ross Sea during the 1994/95 and 1999/2000 seasons; DDT ranged from 0.3 to 0.0670.15 ng g1 wet wt and PCBs from 9.39–138 to 3.5173.03 ng g1 wet wt. HCB levels were similar – being 4.4 and 4.8575.49 ng g1 wet wt, respectively, in the two periods – confirming its worldwide distribution and tendency to accumulate in the polar regions. A dissimilar trend can be observed in the emerald rockcod; samples collected in the same area (Terra Nova Bay, Ross Sea) along a 20-year time span showed a probable decreasing trend from 1987–90 seasons in PCB concentrations. HCB and DDT both decreased from late 1980s to 1995 and then increased again in 2000–02. These trends agreed with that reported for from the Weddell Sea (humped rockcod, mackerel icefish, and blackfin icefish). It is interesting to note that chlorinated pesticides (HCB, DDTs, and CHLs) showed similar concentration and patterns in the 1980–90s period in organisms from the Western and Eastern Antarctica, whereas a clear time trend is not easy to determine in both areas for PCBs. The initial POP decrease observed in many ecosystems around the world was due to their reduced or broken off production and use in industrial countries of North America and Europe. The growing population and industrialization of many developing countries have likely increased the use of many low-cost pesticides and industrial mixtures like DDT and PCBs. The continuing legal or illegal use of many POPs and their release from stocks of unused chemicals may contribute to the continuing emission and distribution of contaminants in the global environments. Many of these compounds show physicochemical properties that allow their global transport; for many of them (e.g., some pesticides and PBDEs), a clear movement toward the polar regions that act as final sink has already been reported as well as their consequent bioaccumulation in polar organisms. On the contrary, PCB and PCDD/F concentrations seem to have declined or remained unchanged in the Arctic since 1980. CHLs, endrin, dieldrin, heptachlor and heptachlor epoxide, mirex, PBDEs, PCNs, PCDDs, and PCDFs were all detected in various species of Antarctic fish. POP and TEQ concentrations in Antarctic organisms are low compared to those reported for marine species from lower latitudes, and they are among the lowest in the world. For instance, the TEQs varied between 0.11 pg g1 wet wt in the muscle of the Antarctic toothfish and 13.76 pg g1 wet wt in the muscle of mackerel icefish, while values may be up to 100 pg g1 in organisms from temperate/tropical regions. The presence of most of the industrial persistent contaminants in the Antarctic fish confirms that Antarctic ecosystems are no longer pristine. Their monitoring will

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Antarctic: Persistent Organic Pollutants and Environmental Health in the Region

be more and more important because of the fragility of trophic webs of such an extreme environment; moreover, the ice caps are a sink for these contaminants that can be released with melting even after the cessation of their use worldwide. Owing to the global warming and the following reduction in ice caps, an increasing amount of contaminants can be released in the seawater and then enter the trophic webs. The extreme weather conditions largely affect the physiology and ecology of organisms; feeding habits, lipid accumulation (strongly linked to food availability during summer months), and long life span may be considered factors of risk. Unusually high concentrations in invertebrates and fish may be of concern not only for organisms themselves but also for top predators, like marine mammals and seabirds (due to biomagnification). The evaluation of POP presence in the tissues of seabirds and marine mammals should be done keeping in mind the migratory habits of the organisms. Some species of penguins and seals spend their entire biological cycles in the Southern Ocean and Antarctic coasts, whereas other species of seabirds and marine mammals (including cetaceans) forage or breed in Antarctic seawaters in summer months and then go northward to overwinter. Thus, their ecology can affect the contaminant body burden a lot; those organisms that forage or breed in the Antarctica during summer and then migrate to northern ranges may accumulate a greater amount of contaminants if they overwinter in polluted areas. Among seabirds, penguins breed on the Antarctic continent or islands and overwinter in the Southern Ocean; therefore, they are very interesting in ecotoxicology because they can be a valid biomonitor of contaminants in the Southern polar region. Petrels, fulmars, and other seabird species that breed in the Antarctic continent or islands can migrate very far from the Southern Ocean. Studies of xenobiotic concentrations in tissues of penguins and flying seabirds have been published since the 1960s, and these articles report data on different families of contaminants (PCBs, DDTs, HCB, HCHs, CHLs, dieldrin, PBDEs, PCNs, PCDDs/Fs, etc.). Most of them report results on the presence of PCBs, HCB, and p,p0 -DDE in various tissues of these birds, and they are very useful to compare results and speculate on the time trend of contamination and health status of Antarctic seabirds. A sample of emperor penguin (Aptenodytes forsteri) fat collected in 1911 and left in an igloo in the Ross Island did not contain any DDT residue. This result has a historic meaning because the sample was collected more than 30 years before the beginning of mass DDT use worldwide. PCBs were detected for the first time in penguin eggs from the Ross Sea region at the end of the 1980s. Samples from the Ross Sea showed a decreasing concentration pattern in the order PCBs 4DDTs 4HCB, whereas in penguins from Antarctic Peninsula, it

was HCB 4DDTs 4PCBs. The abundance of these POPs in organisms from Syowa Station (Indian sector of the Antarctic costs) was similar to that found in the organisms from the Antarctic Peninsula, whereas the profiles in penguins from Davis and Casey stations were similar to that of the Ross Sea. These patterns agreed with those observed in fish and invertebrates from the same regions. It seems that the increasing PCB and decreasing DDT concentrations follow a clockwise and opposite trend. It is likely due to a mix of factors: the different POP global transport paths, the use of different chemicals in various countries, and the movements of air masses within the Southern Hemisphere as well as on a global scale may affect a differential transport and accumulation in the Antarctica. Levels were lower than those detected in other areas of the world, with few exceptions. It is interesting to note that flying seabird species that overwinter north of the Antarctic Convergence showed higher levels than penguins and snow petrels (Pagodroma nivea) that overwinter in the Antarctic seawaters. Moreover, skua eggs collected in the Ross Sea showed the typical pattern observed in this area (PCBs4DDE); in skua and petrel eggs collected in the Antarctic Peninsula or in the Indian sector, the order of abundance was not homogeneous. This may mean that skua breeding in the Ross Sea overwinter in the same sector of the Southern Ocean, migrating to northern subAntarctic islands or to Australian and New Zealander coasts; this migrating behavior was observed in adults, while young specimens can reach the Northern Hemisphere. Migrating seabirds that breed in the other regions of Antarctica may have wider overwintering ranges and reach northern and anthropized lands more easily and rapidly. Interestingly, PCB, DDE, and HCB levels in blood samples of penguins and skuas from both the Antarctic Peninsula and other regions show a profile different from that measured in egg samples; in fact, PCBs made up most of the residue, followed by DDE or HCB (Figure 10). Ade´lie penguins show low capacity to metabolize POPs, compared to South Polar skua and humans. Differences in the accumulation burden and pattern may be due to the specific capacity to metabolize POPs and to the different diets. The knowledge of the detoxifying activity in the other species of penguins is poor. It was reported that the contaminant levels in Ade´lie penguins vary with diet, being higher when specimens feed on krill, a fatty food resource; at the same time, it seems that the contaminant distribution and concentrations in the body vary also with starvation, with muscle and bone accumulating higher levels of POP residues. POPs other than HCB, DDTs, and PCBs have been detected in other tissues of penguins and flying seabirds nesting in Antarctica, and concentrations vary depending

Antarctic: Persistent Organic Pollutants and Environmental Health in the Region Blood

PCBs

p,p’DDE

HCB

DDTs

HCHs

PBDEs

PCDDs

93

PCDFs

1000 100

ng/g wet wt

10 1 Adelie p

Antarctic p

0,1

Gentoo p

2004

0,01

Adelie p 2000_01

Adelie p

Emperor p

2001_02

s.p. skua

s.p. skua

2000_01

2001_02

Ross Sea

Antarctic Peninsula seawaters

Ross Sea

0,001

Figure 10

Concentrations (ng/g wet wt) of some POPs in the blood of penguins and flying seabirds (p = penguin; s.p. = South Polar).

150

Ross sea

Figure 11

Gentoo 62 p

Antarctic 12 p

Adélie p 21

s.p. skua 32

s.p. skua 38

Weddell 18 seal

Weddell 0.65 seal

Adélie p 5

Adélie p 5.9

Adélie p 12

0

Weddell 159 seal

50

s.p. skua 678

100 Adélie p 20

pg g

−1

wet wt

TEQs 200

Antarctic peninsula seawaters

TEQs (pg/g wet wt) evaluated for penguins and seals (p = penguin; s.p. = South Polar).

on the tissue analyzed and the species. Studies published since 1966 report data of POP levels in fat, heart, kidney, liver, lungs, muscle, pancreas, oviduct, and testes, stomach content, guano, and preen gland oil. Concentrations were higher in organisms collected in the Antarctic Peninsula seawaters, followed by those from the Indian sector and finally by those from the Ross Sea. The concentrations in all these species were in the same range of those reported in many flying seabirds that overwinter in non-Antarctic regions and values were lower than in the Antarctic skua (Catharacta antarctica). POPs that were also reported in penguins and flying migrating seabirds nesting in Antarctica were CHLs, PCDDs/Fs, PCNs, PFCs, mirex, and PBDEs. The evaluation of the toxic potential of dioxin-like compounds (PCDDs/Fs, PCB), expressed as TEQs, averaged between 0.65 pg g–1 wet wt in the Weddell seal from the Ross Sea and 679 pg g1 wet wt in the South Polar skua collected in the Ross Sea; different penguin species from the Ross Sea and the South Shetland Island showed TEQ values of the same order of magnitude. TEQs were lower in penguins than in skuas (Figure 11). Levels are lower than those detected in other organisms from tropical and temperate areas of the world, except

for skuas. This pattern is due to the migratory habits of skuas that overwinter in northerly regions. TEQ concentrations found in Antarctic organisms were similar to those reported for three species of seabirds from the Arctic. Marine mammals that breed or feed in Antarctica during summer months spend the rest of the year in Antarctic seawaters or migrate northward depending on the species. For example, the Weddell seal lives its entire life cycle in Antarctic seawaters and gives birth on the pack along the coasts at the beginning of the summer. Cetaceans migrate to tropical regions or to the Northern Hemisphere to overwinter. As well as in birds, the POP accumulation in marine mammals depends on several factors, including specific metabolism. Species and individuals that migrate to anthropized areas are exposed to POPs more than those that stay in Antarctica all around the year. As a consequence, concentrations are quite variable among species, areas, and year of sampling. DDTs, PCBs, and HCB were reported in various species along a 40-year time span; data on the presence of other POPs are scarce. The leopard seal (Hydrurga leptonyx) is likely the species that accumulate mostly in relation to its position in the trophic webs, being a top predator that

94

Antarctic: Persistent Organic Pollutants and Environmental Health in the Region Antarctic Peninsula (fur s = fur seal; leop s = leopard seal; crab s = crabeater seal; Wedd s = Weddell seal; eleph s = elephant seal) DDE

PCBs

DDTs

HCB

lindane

HCHs

600 ng/g wet wt

500 400 300 200 100 fat

fat

fat

fat

blood

fat

fat

fat

crab s

crab s

Wedd s

Wedd s

Wedd s

Wedd s

Wedd s

eleph s

eleph s

Wedd s

Wedd s

Wedd s

1981

1979−81

1981

1985

1990

1990

1993/94

1979−81

2004/05

1981/82

1981/82

1981

fat

fat

leop s 1979−81

fat

fat

fur s 2005

liver

fur s 2004

liver

fur s 1987

fat

fur s 1979−81

fat

fat

0

Antarctic Peninsula (fur s = fur seal; leop s = leopard seal; crab s = crabeater seal; Wedd s = Weddell seal; eleph s = elephant seal) dieldrin

PCNs

PCDDs

PCDFs

PFOS

PFOA

fat

fat

fat

Wedd s

Wedd s

eleph s

eleph s

Wedd s

Wedd s

Wedd s

1990

1990

1993/94

1979−81

2004/05

1981/82

1981/82

1981

fat

fat

Wedd s

1985

fat

Wedd s

1981

fat

Wedd s

1979−81

fat

crab s

1981

fat

crab s

fat

leop s 1979−81

fat

fur s 2005

fat

fur s 2004

liver

fur s 1987

liver

fur s

fat

blood

PFCs

1979−81

fat

ng/g wet wt

CHLs 20 18 16 14 12 10 8 6 4 2 0

Ross Sea (crab s = crabeater seal; Wedd s = Weddell seal; Ross s = Ross seal; mink w = minke whale) DDE

DDTs

PCBs

HCB

HCHs

CHLs

PCNs

PCDFs

PCDDs

2500

ng/g wet wt

2000 1500 1000

Figure 12 seal).

fat

muscle*

liver

crab s

Wedd s

Wedd s

Ross s

Wedd s

Wedd s

crab s

Wedd s

Wedd s

minke w

1964

1964/65

1967

1981/82

1990/91

1995/96

1964

1995/96

1990/91

1984−93

liver

fat

fat

fat*

fat

fat

0

fat

500

Concentrations (ng/g wet wt; * = ng/g lipid wt) of some POPs in the tissues of seals (Wedell s = Weddell seal; Fur s = fur

feeds on penguins and other seals. Those POPs that were detected in its tissues showed the highest levels of DDE, PCBs, and HCB (Figure 12). Another species that seems to accumulate more than the others is the Weddell seal; PCB concentrations were 395 ng g1 wet wt in fat samples collected in 1994/95 in the Ross Sea. CHLs, dieldrin, PCNs, PCDDs/Fs, and PFCs were also detected in this species. Research stations are the only locations where humans live in the Antarctic continent. Usually organic waste is incinerated locally, and plastic, metal, and other nonbiodegradable waste are brought back to the mother or near hosting countries. The release of POPs in the surrounding environments is a normal consequence for scientific stations; plastic and other polluting materials are usually transported to the mother country or the nearest continent for disposal, but a certain emission is possible and may contribute to the local contamination. The incineration of the organic waste may be source of local contamination of dioxins and dioxin-like compounds. The highest impact is reported around McMurdo Station (USA) that is also the biggest one in the Antarctica; PCBs were detected at high and sometime toxic concentrations in bivalves and other benthic

organisms from the McMurdo Sound, with concentration decreasing as long as distance of sampling increases. The impact of Syowa Station (Japan) was reported to be detectable in organisms. DDTs were 2 times higher and PCBs 30 times higher in emerald rockcod samples collected near the station than 10 km far from it. Data related to Arctowski (Poland) and Mario Zucchelli stations (formerly Terra Nova Bay Station, Italy) revealed that these scientific bases showed a low impact in the 1990s.

Conclusive Considerations In general, POP and TEQ concentrations in Antarctic organisms were low compared to those reported for marine species from lower latitudes, and they are among the lowest in the world. The extreme weather conditions largely affect the physiology and ecology of organisms; feeding habits, lipid accumulation (strongly linked to food availability during summer months), and long life span may be considered factors of risk. Unusually high concentrations in invertebrates may be of concern not only for the organisms themselves but also for top predators (due to biomagnification). For example, even

Antarctic: Persistent Organic Pollutants and Environmental Health in the Region

low concentrations of some toxic contaminants may have hazardous effects on penguins: DDE is reported to increase the respiratory rates in the liver mitochondria, and it increases the fat metabolism. Therefore, penguins may be a species at risk because starvation occurs for several weeks during the breeding period and the consequence is an increase and redistribution of POP concentrations in some tissues. Comprehensive datasets of industrial contaminants in Antarctic organisms are available only for few compounds (HCB, DDTs, and PCBs). It is difficult to evaluate a time trend because of the paucity of data. It seems concentrations have increased and decreased during decades (up in the 1970s, down in the 1980s, and up again in 1990), but a clear trend is not evident. Levels of industrial contaminants are highly variable in Antarctic biota, depending on the several factors and likely to the local contamination. Concentrations in some specimens/species were reported occasionally high and comparable to those found in regions with a strong human impact. The increasing concentrations of some POPs in the Arctic, and of the already reported toxic effects in the Arctic biota (e.g., polar bear), may be the confirmation that polar environments are the final sink for some persistent contaminants. Global warming is affecting ice melting in polar regions, and it may be considered a factor of risk in relation to the possible POPs release that are already entrapped in ice. The following increase in newly bioavailable contaminants can affect the health of the fragile Antarctic ecosystems and other unforeseeable effects at a global scale. See also: Singapore: Exposure to Persistent Organic Pollutants and Human Health Risks.

Further Reading Bargagli R (2005) Antarctic Ecosystems, Environmental Contamination, Climate Change, and Human Impact. Heidelberg: Springer-Verlag. Bengtson NSM, Poulsen AH, et al. (2008). Persistent organohalogen contaminant burdens in Antarctic krill (Euphausia superba) from the eastern Antarctic sector: A baseline study. Science of The Total Environment 407(1): 304–314. Corsolini S (2007) Non-pesticide endocrine disrupters and reproductive health. In: Nicolopoulou-Stamati P, Hens L, and Howard CV (eds.) Environmental Science and Technology Library. Reproductive Health and the Environment, vol. 22, pp. 161–186. Dordrecht, the Netherlands: Springer. Corsolini S (2009) Industrial contaminants in Antarctic biota. Journal of Chromatography A 1216: 598–612. Corsolini OS, Ademollo N, Minucci G, and Focardi S (2003) Persistent organic pollutants in stomach contents of Ade’lie penguin from Edmonson Point (Victoria land, Antarctica). In: Huiskes AHL, Gieskes WWC, Rozema J, Schorno RML, van der Vies SM, and Wolff WJ (eds.) Antarctic Biology in a Global Context, pp. 296–300. Leiden, the Netherlands: Backhuys Publishers. Corsolini S, Borghesi N, Schiavone A, and Focardi S (2007) Polybrominated diphenyl ethers, polychlorinated dibenzo-dioxins, -furans, and -biphenyls in three species of Antarctic penguins. Environmental Science and Pollution Research 14: 421--429.

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Corsolini S, Covaci A, Ademollo N, Focardi S, and Schepens P (2006) Occurrence of organochlorine pesticides (OCPs) and their enantiomeric signatures, and concentrations of polybrominated diphenyl ethers (PBDEs) in the Ade´lie penguin food web, Antarctica. Environmental Pollution 140: 371--382. Corsolini S and Focardi S (2000) Bioconcentration of polychlorinated biphenyls in the pelagic food chain of the Ross Sea. In: Faranda F, Guglielmo L, and Ianora A (eds.) Ross Sea Ecology, pp. 575--584. Berlin: Springer-Verlag. Corsolini S, Kannan K, Imagawa T, Focardi S, and Giesy JP (2002) Polychloronaphtalenes and other dioxin-like compounds in Arctic and Antarctic marine food webs. Environmental Science and Technology 36: 3490--3496. Focardi S, Gaggi C, Chemello G, and Bacci E (1991) Organochlorine residues in moss and lichen samples from two Antarctic areas. Polar Record 27: 241--244. Lakaschus S, Weber K, Wania F, Bruhn R, and Schrems O (2002) The air-sea equilibrium and time trend of hexachlorocyclohexanes in the Atlantic Ocean between the Arctic and Antarctica. Environmental Science and Technology 36: 138--145. Montone RC, Taniguchi S, and Weber RR (2001) Polychlorinated biphenyls in marine sediments of Admiralty Bay, King George Island, Antarctica. Marine Pollution Bulletin 42(7): 611–614. Risebrough RW, Rieche P, Peakall DB, Herman SG, and Kirven MN (1968) Polychlorinated biphenyls in the global ecosystem. Nature 220: 1098--1102. Safe S (1990) Polychlorinated biphenyls (PCBs), dibenzo-p-dioxins (PCDDs), dibenzofurans (PCDFs) and related compounds: Environmental and mechanistic considerations which support the development of toxic equivalency factors (TEFs). CRC Critical Review Toxicology 21: 51--88. Sladen WJL, Menzi CM, and Reichel WL (1966) DDT residues in Ade´lie penguins and crabeater seal from Antarctica. Nature 210: 670--673. Subramanian An, Tanabe S, Hidaka H, and Tatsukawa R (1986) Bioaccumulation of organochlorines (PCBs and p,p0 -DDE) in Antarctic Adelie penguins Pygoscelis adeliae collected during a breeding season. Environmental Pollution (Series A) 40: 173--189. Van den Berg M, Birnbaum L, Bosveld ATC, et al. (1988) Toxic equivalents factors (TEFs) for PCBs, PCDDs, PCDFs for humans and wildlife. Environmental Health and Perspectives 106: 775--788. van den Brink NW, van Franeker JA, and de Ruiter-Dukman EM (1998) Fluctuating concentrations of organochlorine pollutants during a breeding season in two Antarctic seabirds: Ade´lie penguin and southern fulmar. Environmental Technology and Chemistry 17: 702--709. Wania F (2003) Assessing the potential of persistent organic chemicals for long-range transport and accumulation in polar regions. Environmental Science and Technology 37: 1344--1351. Weber K, and Goerke H (2003) Persistent organic pollutants (POPs) in Antarctic fish: Levels, patterns, changes. Chemosphere 53: 667– 678.

Relevant Websites http://www.amap.no Arctic Monitoring and Assessment Programme, Oslo, Norway. http://www.anta.canterbury.ac.nz/ University of Canterbury, New Zealand. http://www.antarcticanz.govt.nz British Antarctic Survey, Cambridge, United Kingdom. http://www.antarcticanz.govt.nz Antarctica New Zealand, Christchurch, New Zealand. http://www.ccamlr.org Convention for the Conservation of Marine Living Resources, Hobart, Tasmania, Australia. http://chemfinder.cambridgesoft.com CambridgeSoft Corporation, Cambridge, UK. http://www.epa.gov Environmental Protection Agency, Washington, DC, USA.

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http://www.era.gs Environmental Research & Assessment Ltd., Cambridge, UK. http://www.fishbase.org Froese, R. and D. Pauly Editors, 2010 FishBase. http://www.iarc.fr International Agency for Research on Cancer, Lyon, France. http://www.jstor.org JSTOR, ITHAKA, Ann Arbor, MI, USA. http://www.noaa.gov National Oceanic and Atmospheric Administration, Washington, DC, USA. http://www.penguinscience.com Project leader David G. Ainley, H.T. Harvey & Associates, San Jose, CA, USA.

http://www.pnra.it Programma Nazionale di Ricerche in Antartide/Italian National Program of Research in Antarctica. http://www.pops.int Stockholm Convention, Geneve, Suisse. http://www.scirus.com Elsevier B.V., Amsterdam, The Netherlands. http://www.who.int World Health Organization, Geneva, Switzerland.