Toxic Effects of CONTAMINANTS in Polar Marine Environments Although polar studies have inherent logistic difficulties that increase both their complexity and their cost, the consequences of not obtaining polar-specific information could be catastrophic. PETER M. CH A PM A N GOLDER ASSOCI ATES (CA NADA) M A RTIN J. RIDDLE AUSTR ALI A N A NTARCTIC DIV ISION
COREL
Unique aspects
ota, which similarly require a high degree of environmental protection, include diatoms adapted to low light intensity and represent up to 30% of oceanic phytoplankton productivity (2). These plant cells are grazed on by other fauna, particularly ice amphipods; these, in turn, are fed on by fish, which are preyed on by birds and mammals. This ecosystem disappears during the summer months when the ice melts. Under-ice biota then become either planktonic or benthic, and the food chain shifts accordingly (Figure 1). Although sea ice and icebergs provide habitats critical to food chains, they also destroy other habitats by scraping shores and shallow sea bottoms, changing topography and current regimes, and effectively restructuring biological communities in those areas. Direct abrasion of the shore by sea ice creates a virtually abiotic intertidal zone that is colonized only briefly during the summer by a few fastgrowing species. Iceberg scouring remains among the five most destructive natural events for any ecosystem on earth (3). These physical stresses can confound identification of other stresses, such as anthropogenic chemical contamination.
The marked seasonal variation of solar radiation and cold temperature in polar regions creates important secondary effects on the physical environment and Polar marine biota the associated biota. The marine environments in the The Arctic and Antarctic regions both host a wide vapolar regions are the only parts of the planet domiriety of marine life, including invertebrates, fish, and nated by sea ice for much of the year. Sea ice limits mammals. However, important differences exist. For wind-driven mixing of the water column, restricts example, the benthic biomass of Arctic marine waters light penetration, and causes physical abrasion. As can be up to an order of magnitude less than that in a consequence, growth of plants and animals in polar marine waters is genFIGURE 1 erally very seasonal. When the sea-ice canopy is present, the water column Arctic epontic communities change with the seasons is highly stratified, restricting nutriThe epontic biota, which are the organisms that live in the porous crystalline unent exchange. In addition, the sea ice derside of the sea ice and are unique to polar marine environments, are a major baabsorbs much of the light that would sis for the regions’ food chains. When the ice melts in the summer, the remaining otherwise be available for photosynunder-ice biota then become either planktonic or benthic, and the food chain shifts thesis, further exacerbating the highly accordingly. seasonal differences in light intensity at high latitudes. However, extremely high productivity does occur at particular times and places. For example, when the coastal sea ice clears in the summer, nutrients are released and light simultaneously penetrates deep into the water. In the winter, at highly localized areas, such as the sea-ice edge and within holes called polynyas, wind-driven upwellings create openings in the ice and provide a continual supply of nutrients (1). These high-productivity events and areas are critical to polar marine ecology and require a high degree of environmental protection. The epontic biota, which are the organisms that live in the porous crystalline underside of the sea ice and are unique to polar marine environments, are an important component of the regions’ food chains. These bi© 2005 American Chemical Society
MAY 1, 2005 / ENVIRONMENTAL SCIENCE & TECHNOLOGY ■ 201A
DAVIS MELT ZER, COURTESY OF NATIONAL GEOGR APHIC IMAGE COLLECTION
B
ecause they are so remote from other parts of the world, polar marine environments are unique. These regions are commonly perceived as fragile, yet there is very little scientific basis for such an assessment. Despite their remoteness, the polar regions are increasingly subject to anthropogenic chemical contamination. However, very few empirical data are available on toxic effects to polar marine biota. What data do exist primarily focus on invertebrates and are restricted to just a few contaminants. No specific data exist on toxic responses of polar mammals and birds, and very little published research is available on the effects of persistent organic pollutants (POPs) to any polar species. Typically, exposures or body loads in polar birds and mammals are compared with threshold levels developed from temperate species. As detailed in this article, the lack of conclusive data for these unique regions makes environmental decision making problematic.
Antarctic waters at comparable depths (4). The most abundant and diverse invertebrate groups in Arctic marine waters are bivalve mollusks, polychaetes, echinoderms, amphipods, and isopods, with high population densities of single species. However, shrimps and crabs are poorly represented (5). In the Antarctic, similar groupings occur, but several consistent and conspicuous differences exist between the faunas of the two polar regions. Several important groups are very much more diverse (50–100% richer) in the Antarctic macrobenthos than in the Arctic; these include mollusks, polychaetes, amphipods, bryozoans, sponges, isopods, ascidians, and pycnogonids (6). Other groups, such as the teleost fishes, stomatopods, cirripeds, and decapod crustaceans, have notably low diversity in the Southern Ocean (7, 8), although some are well represented in the fossil record (9). In the popular media, the resident species of polar regions are represented as barely clinging to life in a harsh environment. In reality, the species evolved with the environment and are highly suited to the conditions. It is not yet clear whether species or functional groups within the polar regions are more sensitive to and susceptible to chemical pollution than those from other areas of the globe. Whether they are indeed fragile will depend on many factors, including how polar species react to and interact with their environment and respond to stressors as individual organisms, populations, and communities. Polar organisms have many characteristics peculiar to the region, some of which are likely to influence their sensitivity or susceptibility to contaminants. Many species are long-lived (10, 11) and, in comparison with species from other regions, have a tendency toward gigantism (12). Large size causes a lower surface-area-to-volume ratio, which means slow contaminant uptake compared with temperate biota (13). At the low temperatures typical of polar regions, metabolic rates are slower (14, 15) than in temperate or tropical regions, and total energy usage is reduced (16, 17 ). In general, life-forms with lower metabolic rates accumulate contaminants in tissues more slowly. However, as an adaptation to the seasonal availability of food, polar biota possess relatively high lipid contents for energy storage. Therefore, they take up more of a lipophilic contaminant than biota elsewhere (18). Moreover, lower energy usage may mean that less energy is available for active detoxification and depuration processes. Thus, overall, polar biota are potentially more sensitive, during long-term exposures, to chemical contaminants than temperate or tropical biota. Many benthic species have shortened or eliminated the vulnerable pelagic larval phase (19) and instead retain developing larvae in brood chambers. Development times are longer (20), and fewer, more fully developed young are released (19). But the
brooding process itself represents a vulnerable life stage, and the strategy of direct development from the adults restricts opportunities for dispersion and long-distance recolonization. A possible consequence is that, should a contamination event cause the loss of a population from a local area, recolonization and re-establishment of the population may take considerably longer than in an environment dominated by species with planktonic larvae. Extinction of a link in the food chain would be more serious in polar than in other regions, because lower diversity and simpler food chains could mean that elimination of just a single species could have serious structural and functional consequences for food webs. As a counterargument, the fact that polar marine ecosystems extend over large geographic areas indicates that damage restricted to one area may be repairable by immigration from adjacent areas. This process will, however, be slowed by the regions’ tendency for brooding and direct development of young.
The Antarctic is far
less developed than
the Arctic, although anthropogenic contaminant
sources do exist.
202A ■ ENVIRONMENTAL SCIENCE & TECHNOLOGY / MAY 1, 2005
Anthropogenic contaminants The Antarctic is far less developed than the Arctic, although anthropogenic contaminant sources do exist. Extraction of oil and gas, mining, disposal of nuclear wastes, military activities, and human settlements are not presently permitted in Antarctica, but they are a major feature of the Arctic. However, rich, undeveloped mineral, petroleum, and natural gas deposits exist in the Antarctic. It would be naive to assume that these will always remain unexploited. Indeed, during the negotiations for the Protocol on Environmental Protection to the Antarctic Treaty (the Madrid Protocol) in the early 1990s, a 50-year moratorium on mining was agreed upon as a compromise because the United States did not want to completely foreclose the option of Antarctic development (21). Current activities in the region already contribute to local contamination, including scientific research and support activities, fishing and whaling, and tourism. Both polar regions are subject to exogenous atmospheric contamination originating from the industrialized areas of the world and transported by gas absorption, precipitation, and dry deposition. In addition, both polar regions are subject to inputs of organic (POPs) and inorganic contaminants (22, 23), and some of these inputs are expected to increase over time. Such contaminants may have direct and indirect toxicological effects on polar marine biota, and these effects may not be predicted on the basis of toxicological information from nonpolar areas.
Toxicity testing As a consequence of oil exploration and development in the Arctic, research on the tolerances of resident
biota to oil spills was funded from the 1970s through (28). However, this study provided no information the early 1980s. However, this research centered on possible causes of the observed toxicity, nor did it on undefined “oil”, rather than on specific compoprovide any basis for comparing the responses with nents of the oil, and had no counterpart studies for those of temperate species. the Antarctic. Lack of funding associated with a colSubsequent sediment toxicity tests demonstratlapse of the oil market in the 1980s resulted in a lapse ed that copper and organic carbon, typical Antarctic of research. Marine toxicity testing in the Arctic becontaminants, were toxic to common Antarctic bengan again in the early 1990s, this time followed by thic soft-bottom marine invertebrates (29). Toxicity research in the Antarctic. This second period of reof metals and hydrocarbons to soft-sediment fausearch generally focused on specific contaminants nal assemblages and benthic diatom communities but also included studies on less well defined con(which dominate Antarctic benthic microflora) was taminants. The vast majority of recent marine toxicalso demonstrated at environmentally realistic levity testing has been conducted in the Antarctic. els (30, 31). Unfortunately, the data did not allow for 1970s to early 1980s. During the initial period of comparisons of sensitivities between Antarctic and research, most toxicity tests involved Arctic invertetemperate benthic diatom communities. However, brates. Key findings included recognition that imthe sediment metal concentrations used were below pacts can differ between polar and temperate regions levels that would likely have been toxic to temperbecause of “differences in the fate and duration of ate species. spilled hydrocarbons, in the distribution of populaVarious water-column tests have been conducted tions in vulnerable habitats, in the long-term ecologiwith individual contaminants, including the shortcal consequences of particular sublethal effects, and term toxicity of lead and zinc to Arctic epontic amperhaps most importantly . . . in the rates of habitat phipods and a pelagic mysid, which were found to be and community recovery under Arctic conditions” surprisingly insensitive compared with temperate (4). Researchers speculated that longer exposure organisms (32). The belief that Arctic marine invertimes in cold Arctic waters, particularly under-ice tebrates are generally sensitive to metals has been waters, could increase toxicity. Epontic communiquestioned on the basis of these findings (33). ties were recognized as being particularly vulneraAdditional research assessed the acute toxicity of ble to oil from, for example, a subsea blowout. This five metals, ammonia, fluoranthene, and the stanevent can cause oil to accumulate at the ice–water dard reference toxicant sodium dodecylsulfate to interface; this directly impacts the under-ice comthree Antarctic amphipods in both short- (4-day) munities by physical effects, such as smothering and and longer-term (14-day) exposures (34, 35). The relowering of light penetration, and by toxicity. Parallel searchers found that 14-day exposures were needed field and laboratory studies of oil toxicity to benthic to provide toxicity data comparable to 4-day expoamphipods indicated that toxicity was higher in labosures with temperate organisms. The toxicity of fluratory experiments than that measured in the field; oranthene was markedly increased by ultraviolet mortality appeared to be directly related to the lev(UV) light. Different species showed varying sensiel of oiling and to be caused by physical rather than tivities to the contaminants. toxicological processes (24). After 60 days, differMeasurements of metal toxicity at early life stagent communities recolonized oiled sediments from es of a common Antarctic sea urchin similarly found which organisms had been that longer exposures (20– Fourteen-day exposures 23 days) resulted in higher removed (25). Exposure to crude oil resulted in prematoxicity than shorter exwere needed to provide posures (6–8 days) and reture shedding of eggs and larvae by amphipods (26). lated the longer exposure Because a large proportion toxicity data comparable times to the longer develof Arctic species brood their opment times of Antarctic to 4-day exposures with larvae (36). Embryos were young, premature shedding of young could have more sensitive to copper temperate organisms. and cadmium than temsevere consequences for those populations. Unforperate species but less sentunately, comparisons between the various studies sitive to zinc and possibly lead. (In general, few data conducted in the 1970s through the early 1980s were exist for lead in echinoderms.) “hampered by the lack of experimental standardizaAn Antarctic amphipod was as sensitive to copper tion” (27). and cadmium as temperate amphipods (37 ). Juve1980s to present. Current research involves sednile Antarctic urchins removed from brood pouches iments, individual contaminants in the water colwere similarly sensitive to copper as temperate speumn, and individual contaminants in combination cies (38). However, an Antarctic ophiuroid was less with other stressors in the water column. An initial sensitive to undispersed diesel fuel than a temperstudy involving contaminated Antarctic sediments, ate urchin. the chemical composition of which was unfortuThe combined effects of copper and other stressnately not characterized, demonstrated effects on ors, such as UV-B radiation and food shortage, inthe survival and behavior of various Antarctic bencreased the sensitivity of a common epontic-in-thethic invertebrates and on the survival of benthic winter and shoreline-in-the-summer amphipods in communities transplanted to contaminated sites the laboratory (39). Under natural conditions, these MAY 1, 2005 / ENVIRONMENTAL SCIENCE & TECHNOLOGY ■ 203A
organisms may reduce their exposure to UV-B by behavioral responses, such as avoidance, or physiological processes, such as increased pigmentation. In the field, the same amphipod, held in aquaria on the sea ice and supplied with water pumped from the water column, showed higher mortality rates in the presence of UV radiation alone and in the presence of mixtures of metals released from a point source (40). This study also demonstrated increased sensitivity to the mixture of metals in the presence of UV radiation. Although these in situ exposures were artificial and not reflective of actual field conditions (e.g., avoidance was not possible), the researchers speculated that toxicity to metals, alone or in combination with UV radiation, could explain the absence of this species in metal-contaminated shallow waters.
Sensitive invertebrates Although polar organisms may be exposed to a wide variety of contaminants, quantitative short-term toxicity data for specific contaminants only exist for five metals (32–38). Data are available (though not for all metals) for just three Antarctic and four Arctic amphipods, two Arctic mysids, and three Antarctic echinoderms. Table 1 shows the limited number of substances and organisms tested; thus, broad generalizations are precluded. For instance, no threshold data exist for POPs. An important practical question related to contaminant sensitivities in polar environments is whether temperate environmental quality criteria and guidelines are sufficiently protective. To address this issue, the available polar toxicity data
were compared with temperate marine water quality guidelines and criteria for Canada, the United States, Australia, and New Zealand. On the basis of short-term tests, such as 1-day and 4-day lethal concentration 50 (LC50) in water and 6–8-day effective concentration 50 (EC50) or no-observed-effect-concentration (NOEC) values shown in Figure 2, polar marine invertebrates tested to date would be protected by the U.S. EPA acute criteria for all five metals (41). The lowest margin of safety would be for copper and the greatest for lead. On the basis of the longer-term tests, as shown in Figure 3 (see p 206A), polar marine invertebrates tested to date might not be protected by the combined temperate chronic guidelines/criteria for copper but would be for cadmium and zinc (34–39). Although these conclusions are only preliminary, data from the Antarctic do indicate a relatively higher sensitivity of polar biota to copper than to cadmium, chromium, zinc, or lead. Therefore, on the basis of these very limited comparisons between the sensitivities of polar and temperate species to specific toxicants (32, 36–38), polar species may be similarly sensitive or more sensitive to copper, variably sensitive to cadmium and zinc, and less sensitive to lead. Despite the limited amount of data, what is clear at this point is that polar marine organisms have consistently longer acute response times. For this reason, comparisons between the acute response of polar and temperate marine biota should be based on similar portions of the toxicity curve, which can mean comparing 14day LC50 results for polar organisms with 4-day LC50 results for temperate organisms. Longer response times for polar marine biota are probably due to the
TA B L E 1
Polar marine toxicity testing conducted to date Polar region
Taxonomic group
Arctic
Antarctic
Species
End points
Contaminants
Amphipod
Onisimus affinis, O. litoralis, Gammarus setosus, Anonyx nugax, A. makarovi
Survival, locomotor activity, growth
Zinc, lead, petroleum hydrocarbons, crude oil
Mysid
Mesidotea entomon, Mysis oculata
Coelenterate
Halitholus cirratus
Amphipod
Orchomene plebs, Orchomenella pinguides, Heterophoxus videns, Monoculodes scabriculosus, Paramoera walkeri
Tanaid
Nototanais dimorphus
Cumacean
Eudorella splendida
Echinoderm
Abatus shackletoni, A. nimrodi, A. ingens, Sterechinus neumayeri, Ophiura crassa
Macroalgae
Desmarestia menziesii, Himantothallus grandifolius, Iridaea mawsonii
204A ■ ENVIRONMENTAL SCIENCE & TECHNOLOGY / MAY 1, 2005
Contaminated sediments, Survival, burial, copper, cadmium, zinc, development, movement, chlo- lead, chromium, sorophyll fluoresdium dodecylsulfate, cence, changes ammonia, fluoranthene, in microbial oil, diesel, chemical oil communities dispersant
Concentration (�g/L)
low ambient temperature, FIGURE 2 which results in both a low metabolic rate and slow upTemperate criteria protect polar regions in the short term take kinetics. For those species exhibiting gigantism, Can the same environmental quality criteria and guidelines be used in temperate and polar clitheir low surface-to-volume mates? According to these polar short-term toxicity data (32–38, 41), the polar marine inverratio may further add to the tebrates tested to date are protected by the EPA criteria for these five metals. LC 50 are 1-day response time (13, 42). Howand 4-day 50% lethal concentration in water, EC 50 is the 6–8-day 50% effective concentration, ever, the effect of gigantism and NOEC is the no-observed-effect concentration. remains untested, as most of 1,000,000 the toxicity tests undertaken so far with polar organisms have used species that are 100,000 similar in size to their temperate analogs. Invertebrates have lon10,000 ger development times in polar regions than in tem1000 perate ones. For example, polar urchins require 2–10 more development time. 100 Thus, in the case of chronic exposures, comparisons between development stages 10 are more ecologically relevant than exposures for 0 fixed times (36). In princiCopper Cadmium Chromium Zinc Lead ple, the ecological significance of toxicity test data U.S. EPA Acute LC50 LC50> EC50 NOEC and the end points used must be considered in the context of the particular environment under consideration. Organisms may be well adapted to environation. For example, because of wind-driven mixing, mental factors that fluctuate across a wide range if extended exposure of echinoderm larvae to a conthey do so predictably. Unpredictable fluctuations, taminant for as long as 20 days is unlikely in many either the occurrence of rare and random events or high-energy temperate or tropical coastal locations. environmental conditions beyond the normal range However, in polar regions, where sea-ice cover preof variation, can create additional stress. vents wind-driven mixing for many months of the As yet, the implications of environmental flucyear, extended exposure is expected. tuations, stability, and predictability to the toxic responses of polar species can only be hypothesized. Effects of fluctuations For example, with the exception of hydrothermal Whether environmental fluctuations ameliorate vent areas (43), polar marine water temperatures or enhance the overall susceptibility of polar speare relatively constant. In many polar locations, cies remains unanswered. Some conditions in the temperatures throughout the year range from about polar marine environment are more constant and –1.85 oC to little more than +1 oC. In absolute terms, predictable than elsewhere; however, in other rethis range is far narrower than that of most temperspects, conditions are very variable. In areas with ate and tropical locations. However, because temenvironmental fluctuations, additional stressors in peratures are so close to the freezing point, slight the form of chemical contaminants could cause mavariations may have disproportionate effects. The jor disruptions of populations and food chains. Alkinetics of many chemical reactions become nonternatively, in areas with more constant conditions, linear as the system approaches a phase change, biota could be less adaptable to unexpected stresssuch as the transition of water from liquid to ice. ors such as chemical contaminants. Slight temperature differences in this range may Some fluctuations occur very predictably in analso have significant and disproportionate influnual cycles, such as scouring of the intertidal zone ence on biological processes, such as the properties by sea ice and the seasonal melting and breakup of of cell membranes. the ice pack, with a concomitant release of nutrients, At high latitudes, the solar cycle varies dramatpenetration of light, and peak in primary production. ically, although the incident light gradually and Other fluctuations, such as scouring of the shallow predictably changes from 24-h darkness in winter benthos by icebergs, vary in the short term. (Howto 24-h daylight in summer. The sudden exposure ever, over the long term, icebergs are a predictable to light superimposes another issue: As the sea ice aspect of life in polar regions.) The predictability of breaks up and drifts away, phototoxicity due to abfluctuations is an important additional considersorption of UV light energy can substantially inMAY 1, 2005 / ENVIRONMENTAL SCIENCE & TECHNOLOGY ■ 205A
FIGURE 3
Over the long term, temperate guidelines may not protect polar regions Comparison of polar longer-term marine invertebrate toxicity data (34 –39 ) for three metals with the range of U.S. EPA chronic values (41), Canadian Council of Ministers of the Environment values (48 ), and Australian and New Zealand Environment and Conservation Council/ Agriculture and Resource Management Council of Australia and New Zealand trigger values (49 ) for 80–99% protection. LC 50 are 1-day and 4-day 50% lethal concentration in water, EC 50 is the 6–8-day 50% effective concentration, and NOEC is the no-observed-effect concentration . 100,000
Concentration (�g/L)
10,000
1000
Peter M. Chapman is a senior environmental scientist at Golder Associates, Ltd., in Canada. Martin J. Riddle is the program leader of the Human Impacts Research Program at the Australian Antarctic Division. Address correspondence regarding this article to Chapman at pchapman@attglobal. net.
100
10
0 Copper Range of chronic guidelines/criteria
Cadmium LC50
Zinc LC50 >
crease the toxicity of PAHs to Antarctic amphipods (34, 35) and presumably would have a similar effect on other polar fauna. Although the ecological relevance of this phenomenon remains to be generally established (44), it could be particularly important in polar regions (36). Further, increased UV-B exposure can substantially increase sensitivities to metals (39) and possibly to other contaminants.
Go north—or south In a recent review of Arctic research, Fisk et al. state: “There have been few studies on the biological effects of contaminants in Arctic organisms from Canada or the circumpolar Arctic. . . . A future area of effects studies and risk assessment should focus on thresholds for Arctic species” (45). Similar comments apply to Antarctic species (46). Although polar studies have inherent logistic difficulties that increase both their complexity and their cost, the consequences of not obtaining the polar-specific information necessary for informed decision making could be catastrophic for those marine ecosystems. To avoid the costs of site-specific testing, managers commonly ask whether they can use temperate data to predict the responses of polar marine organisms to contaminants and use temperate criteria and guidelines to protect them from 206A ■ ENVIRONMENTAL SCIENCE & TECHNOLOGY / MAY 1, 2005
EC50
those contaminants. Based on the very limited data available, the only answer possible to such questions is “yes” in some cases but “no” in others—and we presently cannot be sure which are which. All the current challenges to ecotoxicology relevant to temperate ecosystems, such as hormesis and ecological complexity, also apply to polar regions (47 ). To adequately address these challenges, we need to undertake more basic research on the ecology of polar marine environments, develop toxic-effects information, and understand how toxicity is modified under the peculiar conditions characteristic of polar regions.
NOEC
Acknowledgment
We thank Chris Hickey for cheerfully digging up his old data files to answer our questions.
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