Trace metals in Antarctic organisms and the development of circumpolar biomonitoring networks

Our present knowledge of Antarctic ecosystems is probably still insufficient to interpret and monitor early ecologically significant effects of climate change and local or remote human activities. With regard to metals of toxicological and environmental concern, available data from snow samples indicate that their biogeochemical cycle only changed in restricted areas (within a few hundred meters or a few kilometers of human settlements). Only Pb and perhaps Cu show some perceptible indication of large-scale alterations caused by anthropogenic emissions in Antarctica and elsewhere in the Southern Hemisphere. In any case, the Antarctic continent and surrounding Southern Ocean are in relatively pristine environmental condition. It has therefore been supposed for many years that because Antarctic organisms evolved in isolation, they were not exposed to and were not adapted to cope with enhanced bioavailability of toxic metals in their environment. Data summarized in this review seem to deny this supposition, showing widespread accumulation of two of the most toxic metals (Hg and Cd) in marine organisms (benthic and pelagic) and cryptogams from icefree areas of Victoria Land. There have been few studies on the ecotoxicology of metals in Antarctic organisms, but available data provide no evidence that these are more sensitive to metals than related species from temperate seas. Indeed, some of the highest concentrations of Hg and Cd ever reported have been measured in tissues of apparently healthy vertebrates from the Southern Ocean. As in other marine areas of enhanced upwelling, the surface waters of the Southern Ocean have high Cd concentrations in spring, at the beginning of the algal bloom, and the metal is adsorbed or absorbed by phytoplankton and zooplankton. Some species of crustaceans (e.g., caridean decapods and hyperiid amphipods), which are important components of the diet of cephalopods, seabirds, seals, and whales, have very high concentrations of Cd. This metal therefore accumulates in the liver (or digestive gland) and kidney of animals feeding mostly on crustaceans, reaching very high values in southern minke whales and several species of albatrosses, petrels, and seals. Most Antarctic marine organisms are probably well adapted to naturally high Cd bioavailability. In fact, in coastal ecosystems, which are often characterized by a low zooplankton biomass, most of the phytoplankton and ice algae sink, transferring Cd to the rich benthic communities. Many invertebrates such as sponges, scallops, and clams consequently show much higher concentrations of Cd than related species from other coastal ecosystems, even those polluted with metals from anthropogenic sources. Unlike Cd, there is no evidence of enhanced Hg bioavailability in Southern Ocean waters. In all aquatic ecosystems, however, inorganic Hg may be methylated to methylmercury (MeHg), which is magnified in food chains. In the oceanic province of the Southern Ocean, most food webs are short and relatively simple (the krill system) and high levels of MeHg accumulate, for example, in long-living birds that feed on organisms that already have preconcentrated MeHg (fish, squid, crustaceans). The bioaccumulation of Hg in bird tissues also occurs because the feathers are an important excretion route of MeHg and, in the Southern Ocean, albatrosses and petrels change their feathers over a period of years rather than annually. In shelf waters around Antarctica, the involvement of benthic organisms in the transfer of energy and trace metals from phytoplankton and other autotrophic organisms to fish, nesting seabirds, and seals lengthens the food chains and enhances the biomagnification of MeHg. Thus, the south polar skua and other predators such as leopard seals may accumulate Hg at levels corresponding to those usually reported in related organisms from polluted environments in the Northern Hemisphere. However, owing to peculiar environmental characteristics of the Southern Ocean, such as the temperature regimen and the seasonal nature of primary production, Antarctic organisms generally have lower growth rates and longer lifespans and molting cycles (crustaceans and seabirds) than do related species from temperate seas. As these factors contribute to enhance the bioaccumulation of metals, ecophysiological differences should be considered when comparisons are made between organisms from the Southern Ocean and other seas. Comparisons could be quite difficult, even among Antarctic organisms, because water masses in the Southern Ocean may show significant spatial and temporal variations in metal concentrations. Besides descriptive baseline data, this review provides indications about widespread species of Antarctic organisms (e.g., Iridaea cordata, Adamussium colbecki, Laternula elliptica, Paramoera walkeri, Trematomus bemacchii) that could be used as reliable biomonitors of metal pollution in coastal ecosystems affected by wastewaters from scientific stations. For the purposes of a circumpolar biomonitoring network, several biotic and abiotic factors affecting the bioaccumulation of metals are also discussed. Less than 2% of continental Antarctica is icefree in summer and most deglaciated areas are barren ground with frost-shattered rocks. However, where some free water is available, even for very short periods, sparse cryptogamic flora of limited taxonomic diversity and low structural complexity may develop. These terrestrial ecosystems are a natural laboratory to study the cycling of macroand microelements between abiotic and biotic components, and the elemental composition of mosses or lichens could be a very useful indicator of changes in the environmental biogeochemistry of metals caused by possible changes in atmospheric precipitation, water availability, leaching, and drainage or the impact of human activities. Unlike snow samples, the most widespread species of Antarctic lichens and mosses do not show deposition of Pb and Cu from remote anthropogenic sources; indeed, concentrations of these elements in Antarctic cryptogams are among the lowest ever reported in related species from other remote areas. Well-developed moss and lichen communities in coastal icefree areas receive most elements from the marine environment through snow, aerosols, and the guano of seabirds. Like marine organisms, Antarctic cryptogams therefore have quite high Cd concentrations. Most scientific stations are concentrated in coastal icefree areas, and changes in the biodiversity of indigenous flora and fauna could be a valuable indicator of the impact of human activities. Moreover, some species of macrolichens and mosses could be useful for establishing long-term biomonitoring networks of trace metal or other persistent atmospheric pollutants around Antarctic stations. When indigenous crytpogams are lacking,-short-term "active" biomonitoring can be performed by transplants (i.e., the moss-or lichen bag technique). Changes in the composition of planktonic microbial communities and the elemental composition of benthic algal mats in small lakes and pools of continental Antarctica may also provide other early warning signals of perturbations or changes in the environmental biogeochemistry of icefree areas. © Springer-Verlag 2001.