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Working_ecol

Endocrine-Disrupting Chemicals and Climate Change: A Worst-Case
Combination for Arctic Marine Mammals and Seabirds?

Bjørn Munro Jenssen
Department of Biology, Norwegian University of Science and Technology, Trondheim, Norway hormone transport proteins, or abilities to The effects of global change on biodiversity and ecosystem functioning encompass multiple complex
disrupt hormone metabolism, many POPs can dynamic processes. Climate change and exposure to endocrine-disrupting chemicals (EDCs) are cur-
mimic or in some cases block the effects of the rently regarded as two of the most serious anthropogenic threats to biodiversity and ecosystems. We
endogenous hormones. In either case, these should, therefore, be especially concerned about the possible effects of EDCs on the ability of Arctic
marine mammals and seabirds to adapt to environmental alterations caused by climate change.
endogenous hormones and, thus, have become Relationships between various organochlorine compounds, necessary such as polychlorinated
biphenyls, dichlorophenyldichloroethylene, hexachlorobenzene, and oxychlordane, and hormones in
(EDCs) (Colborn et al. 1993). Examples of Arctic mammals and seabirds imply that these chemicals pose a threat to endocrine systems of these
environmental pollutants with endocrine-dis- animals. The most pronounced relationships have been reported with the thyroid hormone system,
rupting properties are some OC pesticides, but effects are also seen in sex steroid hormones and cortisol. Even though behavioral and morpho-
phthalates, alkylphenolic compounds, PCBs, logical effects of persistent organic pollutants are consistent with endocrine disruption, no direct evi-
dence exists for such relationships. Because different endocrine systems are important for enabling
animals to respond adequately to environmental stress, EDCs may interfere with adaptations to
metals, including lead, mercury, and cadmium increased stress situations. Such interacting effects are likely related to adaptive responses regulated
(Crisp et al. 1998; Meerts et al. 2001). It by the thyroid, sex steroid, and glucocorticosteroid systems. Key words: glaucous gull, Haliocherus,
should also be noted that Arctic marine mam- Larus hyperboreus, PBDEs, PCB, polar bears, POPs, seal, Ursus maritimus. Environ Health Perspect
mals and seabirds have the ability to metabolize 114(suppl 1):76–80 (2006). doi:10.1289/ehp.8057 available via http://dx.doi.org/ [Online
many POPs to more polar forms that contain 21 October 2005]
hydroxy groups via the hepatic cytochromeP450 enzyme system. Paradoxically, many ofthe metabolites formed during phase I or II Before the 17th century the anthropogenic to physical, chemical, and biochemical degra- metabolism have endocrine-disrupting proper- impact on Arctic ecosystems was restricted to dation and, therefore, remain available for ties (van den Berg et al. 2003). Thus, a well- a sustainable level by a very limited number of uptake and bioaccumulation for a long period indigenous inhabitants, and most of the Arctic of time. Thus, they have a potential for long- guarantee against endocrine-disrupting effects was untouched by humans. As a consequence range environmental transport, and they have adverse effects (Stockholm Convention 2005).
Northwestern passages by scientific and mer- nized as another significant threat to Arctic bio- cantile expeditions, the vast natural resources mammals and seabirds are industrial organo- diversity and ecosystem functioning. Although in the Arctic ecosystem were discovered. The debate is ongoing as to the causative factors exploitation of these resources has resulted in biphenyls (PCBs), hexachlorobenzene (HCB), with respect to the climate change issue, there is polychlorinated dibenzo-p-dioxins (PCDDs) clear evidence of the ecological impact of recent marine mammal species and populations such and polychlorinated dibenzofurans (PCDFs), climate change, from polar terrestrial to tropical as the Steller’s sea cow (Hydrodamalis gigas), and polychlorinated naphthalenes (PCNs), as the bowhead whale (Balaena mysticetus), and well as OC pesticides such as dichlorophenyl- et al. 2001; Moritz et al. 2002; Overpeck et al.
the walrus (Odobenus rosmarus). Within a cen- trichloroethane (DDT) and its metabolites, 1997; Rind 2002). The responses of both flora tury, the characteristics and function of the chlordane, heptachlor, dieldrin, endrin, and and fauna span an array of ecosystems and Arctic ecosystem were dramatically changed, organizational hierarchies, from the species to and they have never recovered. Even today Programme 2004). Recently, several so-called the community levels (Stenseth et al. 2002; there is considerable concern within the scien- novel POPs such as polybrominated diphenyl Walther et al. 2002). Several reports emphasize tific community, government regulators, and ethers (PBDEs) and perfluorooctane sulfonate that high-latitude regions are particularly sus- the public about the impact of direct human ceptible to climate change (Moritz et al. 2002; activities such as hunting, fishing, and habitat Overpeck et al. 1997). Case studies, especially change and/or destruction on Arctic biodiver- Kannan 2001; Herzke et al. 2003; Ikonomou in the marine environment, have indicated that et al. 2002; Wolkers et al. 2004). The concen- climate change can reinforce the detrimental trations of some of these compounds such as This article is part of the monograph “The long-range atmospheric transport of manmade marine mammals (Ikonomou et al. 2002).
Ecological Relevance of Chemically InducedEndocrine Disruption in Wildlife.” Thus, even though there is evidence that levels organic pollutants (POPs) were detected in of classic POPs such as PCBs are decreasing or Department of Biology, Norwegian University of endemic Arctic species, such as polar bears have leveled off [for example, as reported in Science and Technology, NO-7491 Trondheim, (Ursus maritimus) (Norheim et al. 1992), polar bears from the Svalbard and Barents Sea Norway. Telephone: 47 7359 6267. Fax: 47 7359 glaucous gulls (Larus hyperboreus) (Bourne and region (Henriksen et al. 2001)], it is likely 1309. E-mail: bjorn.munro.jenssen@bio.ntnu.no that the total exposure of Arctic biota to POPs This publication was financed by Norwegian Research Council project no. 155933/S30.
Arctic phocids (Bang et al. 2001), and beluga will increase during the next decade.
The author declares he has no competing financial whales (Delphinapterus leucas) (Andersen et al.
2001). POPs are chemicals that are resistant endogenous hormones, abilities to interact with Received 31 January 2005; accepted 13 June 2005.
VOLUME 114 | SUPPLEMENT 1 | April 2006 • Environmental Health Perspectives Endocrine-disrupting chemicals and Arctic climate change effects of human impact and push species and In a series of articles Bustnes and co-workers temperate waters. Because many of these species ecosystem tolerances over their limits (Planque have focused on ecological effects of OCs in also inhabit Arctic waters, I have chosen to and Frédou 1999). Biomagnification of many glaucous gulls from Bear Island. The propor- include some of the main findings from these POPs is particularly high for marine endother- tion of time that adult glaucous gulls were studies here. In ribbon seals (Phoca fasicata) mic animals (Hop et al. 2002); these animals absent from the nest when not incubating and from Japanese waters, TT3 levels decreased sig- are also among the most vulnerable to climate the total number of absences were both signifi- nificantly with increased blubber concentra- cantly related to blood concentrations of PCB The effects of global change on biodiver- (Bustnes et al. 2001). The authors suggested such relationship was found between blubber that the effect could be apparent because indi- PCBs and FT3 (Chiba et al. 2001). In Larga multiple complex dynamic processes. Climate viduals with high blood concentrations of OCs seals (Phoca largha), also from Japanese waters, change and exposure to EDCs are currently need more time to gather food as a result of plasma TT3 and FT3 correlated negatively with regarded as two of the most serious anthro- either endocrine disruption or neurological dis- blubber PCB concentrations, whereas no such pogenic threats to biodiversity and ecosystems.
orders. Furthermore, females with high blood relationships were found between blubber PCB We should, therefore, be especially concerned levels of OCs, including HCB, oxychlordane, about the possible effects of EDCs on the abil- dichlorophenyldichloroethylene (DDE), and Larga or ribbon seals (Chiba et al. 2001).
ity of Arctic marine mammals and seabirds to PCBs, were more likely to have nonviable eggs For gray seal (Halichoerus grypus) pups adapt to environmental alterations caused by from the United Kingdom, there was generally climate change. My aim in the present article (Bustnes et al. 2003). Adult yearly survival rate is to give a short review of the effects of EDCs was also reported to have a significant negative through mother’s milk or between PCB con- on Arctic mammals and seabirds, and to assess relationship to blood concentrations of DDE, centrations in blubber and plasma levels of the possible interactions between climate persistent PCBs, and HCB, and especially to TT4, FT4, TT3, or FT3 (Hall et al. 1998). In oxychlordane (Bustnes et al. 2003). Bustnes captive harbor seals (Phoca vitulina) de Swart and co-workers also reported a significant posi- Endocrine Disruption in Arctic
tive relationship between wing feather asym- ured after fasting was lower in seals fed herring Marine Mammals and Seabirds
metry (difference between the length of right from the Baltic Sea than in the control seals fed Chemical pollutants can disrupt endocrine and left wing feathers) and blood concen- cleaner herring from the open waters of the function in animal groups ranging from inver- trations of two PCB congeners (PCB-99 and Atlantic Ocean. In a similar feeding experi- tebrates, amphibians, and reptiles to birds and PCB-118), oxychlordane, DDE, and especially ment, captive harbor seals given a diet of OC- contaminated fish had significantly lower plasma levels of TT4, FT4, and TT3 compared Verslycke et al. 2004; Vos et al. 2000).
regulating the molting and replacement of with seals fed with less contaminated fish Although most of the endocrine-disrupting (Brouwer et al. 1989). Sormo et al. (2005) properties of chemicals have been documented 2004). As noted above, significant negative found that gray seal pups from the Baltic Sea through experimental exposure of animals, relationships between plasma concentrations have lower plasma concentrations of TT3 and there is an increasing number of studies in FT3 compared with pups from the Norwegian which disruptions or alterations in reproduc- been reported in glaucous gulls (Verreault Sea, whereas there was no difference in plasma tive activity, morphology, or physiology have et al. 2004). Thus, a link may exist between concentrations of TT4 and FT4 between the been reported in wildlife populations (Guillette the TH-disruptive effects of HCB and oxy- two groups. Because concentrations of OCs in and Gunderson 2001; Vos et al. 2000). The chlordane and the growth and development of blubber were significantly higher in the Baltic modes of action by which the chemicals exert the primary wing feathers following molting.
group than in the Norwegian group, the results their endocrine-disruptive effects have been There is a high aerodynamic cost of asym- can be interpreted as a strong indication that described in many of the studies and reviews metry (Thomas 1993), and Bustnes et al.
listed above, and will not be elucidated here. In (2001) suggested that increased flight costs affected by the exposure of young phocids to several recent studies and reviews, the links may be an important factor in explaining why OCs. Furthermore, stranded immature north- between endocrine disruption, particularly of birds with high blood concentrations of POPs ern elephant seals (Mirounga angustirostris) the thyroid system, and neurodevelopment and spend more time on feeding trips than birds with a skin disease had elevated serum levels of cognitive effects have received attention with low levels (Bustnes et al. 2001). Exposure to PCBs has been associated with cognitive and TT4 compared with those in unaffected and behavioral changes (Jacobson et al. 1990; controls (Beckmen et al. 1997). In northern The glaucous gull is a top predator in the Schantz 1996; Sher et al. 1998), and it has fur seal (Callorhinus ursinus) neonates, TT4 was Arctic food web, and high levels of POPs have been suggested that the effects of PCBs on reported to correlate negatively with several been reported in this species (Bourne and brain development may be attributable, at PCB congeners (Beckmen et al. 1999).
Bogan 1972; Gabrielsen et al. 1995).
least in part, to their ability to affect the thy- Ikonomou et al. (2002) reported increasing Verreault et al. (2004) reported significant roid system (Zoeller 2001; Zoeller et al.
levels of brominated flame retardants such as negative relationships between plasma levels of 2002). It is, therefore, tempting to speculate PBDEs in Arctic ring seals (Phoca hispida); in gray seals, Hall et al. (2003) found that TH trations of free thyroxin (FT4) and total thy- the ultimate cause of this altered parental levels may be affected by PBDEs. Thus, it is roxin (TT4) in adult breeding glaucous gull behavior. However, more research into linking important to include novel POPs when assess- males from Bear Island (Bjørnøya) in the endocrine disruption to behavioral and eco- ing the effects on endocrine disruption.
Barents Sea. Furthermore, negative correla- logical alterations in free-living animals is The polar bear is the ultimate apex preda- tions were found between several other OCs needed before conclusions regarding this feed- tor in the Arctic food chain. Even though the and the FT4:free triiodothyronine (FT3) and polar bear has a relatively well-developed TT4:total triiodothyronine (TT3) ratios in capacity for metabolizing and excreting POPs males. No effects were found in females.
studied in several species of phocid seals from (Bernhoft et al. 1997), this animal accumulates Environmental Health Perspectives • VOLUME 114 | SUPPLEMENT 1 | April 2006 relatively large amounts of POPs because it in the projected trends of global warming, of physiological processes including reproduc- feeds almost exclusively on large amounts of ecological responses to recent climate change seal blubber (Derocher et al. 2002). During the are already clearly visible (Stenseth et al. 2002; (Wingfield and Sapolsky 2003). These hor- last decade, Skaare and co-workers have con- mones are also important in the regulation of ducted a series of studies on the accumulation Changes in species abundances and distri- and effects of POPs in polar bears from the bution in migratory species are among the In polar bears, learning and cognitive abili- Svalbard and the Barents Sea region. They best-documented effects of climate change ties are probably important factors for success- found significant relationships between POPs (Crick and Sparks 1999; Easterling et al.
ful hunting. There is concern that disruption and THs and vitamin A (Skaare et al. 2001).
2000). Climate change has affected the repro- of the TH balance by EDCs may affect neuro- In a recent study (Braathen et al. (2004) these ductive grounds of krill (Euphausia superba) development, and that this outcome in turn relationships were studied in more detail, and and, consequently, its recruitment, by reduc- may affect behavior and cognitive abilities of it was found that PCBs affected five TH vari- wildlife (Jenssen 2003). It is therefore possible ables in females (TT4, FT4, FT3, TT3:FT3, that EDCs affect behavior and cognitive abili- et al. 1997). Karnovsky et al. (2003) reported ties in polar bears such that they are less able to (FT3, FT4:FT3). These results indicate that that little auks (Alle alle) at Svalbard feed cope with changes in ice-coverage caused by female polar bears could be more susceptible mainly on the large copepod (Calanus climate change. Bustnes et al. (2001) reported than males to TH-related effects of POPs. The glacialis), restrict their foraging activity to a correlation between levels of OCs and behav- actions of THs are mediated by nuclear TH Arctic water that contains this copepod, and ior in glaucous gulls. In a temporal and/or spa- receptors that have their highest affinity for avoid Atlantic water that contains a smaller tial change in the distribution of food caused copepod (Calanus finmarchicus). They argued by climate change, an altered behavior caused noting that in polar bears, PCB was reported that these little auks may be affected by cli- by EDCs could hamper the breeding success or to have a greater effect on T3 than on T4 mate change because during years when the even the survival rates of adult glaucous gulls.
(Braathen et al. 2004). Furthermore, in female flow of Atlantic water increases, they may be It is possible that the behavioral changes in polar bears, plasma progesterone levels were forced to forage in areas with suboptimal con- glaucous gulls are linked to an increase in positively correlated with plasma concentra- energy expenditure caused by increased rates of tions of PCBs (Haave et al. 2003). Increased asymmetry in highly polluted gulls (Bustnes levels of progesterone may disturb the normal birds breed earlier. Negative relationships et al. 2002). Because THs are important in reproductive cycle of the females, thereby hin- between sea temperature and hatching date feather growth after molting, it is possible that dering successful mating. In male polar bears, have been reported for several seabird species plasma concentrations of both OC pesticides (Bertram et al. 2001; Durant et al. 2004; involved in the reported wing asymmetry in and PCBs contributed negatively to the plasma Gjerdrum et al. 2003). Thus, when sea tem- glaucous gulls (Verreault et al. 2004). In com- testosterone levels (Oskam et al. 2003); thus, it perature increases because of climate warming, bination with a climate-induced spatial change is possible that male reproductive performance it is likely that the breeding and hatching in the availability of food resources in relation is affected by POPs. Recently, relationships starts earlier. Extensive studies of large mam- to breeding areas, additional effects of EDCs between blood levels of OCs and cortisol levels mals indicate that climatic extremes influence on morphological features may result in even have also been documented in polar bears from juvenile survival, primarily during winter, higher energy demands for feeding. This effect Svalbard and the Barents Sea (Oskam et al.
may cause a further decrease in the breeding 2004). The OC pesticides contributed nega- density (Milner et al. 1999; Post and Stenseth success of polluted glaucous gulls. Conversely, tively, whereas PCBs contributed positively to 1999). The ice-edge is a particularly produc- if climate change results in an allocation of the variation in plasma cortisol. The authors tive area, and for Arctic seals it is apparent that food closer to the breeding areas, the func- do, however, report that the overall contribu- the loss of ice will reduce the availability of tional effects of wing asymmetry could lessen, tion of the POPs to the cortisol levels was neg- areas for efficient feeding, haulout possibilities, and even highly polluted birds might be able to ative. It is possible that the altered plasma and breeding. For the polar bear, reduced ice- cortisol levels inhibit physiological processes coverage in the Arctic will reduce their possi- In the Arctic the summer season is short, involved in homeostasis and thereby render the bilities for hunting seals. Also, lowered seal and proper timing of breeding, molting, and populations would most likely affect hunting migration is important for seabirds. Exposure success and survival and in turn populations of to EDCs could disrupt the endocrine systems and mechanisms that regulate these events, Climate Change
thereby leading to suboptimal timing in rela- Possible Combined Effects of
tion to the season. However, because the most approximately 0.6°C over the past 100 years.
EDCs and Climate Change
In Artic marine mammals and seabirds, THs, change is climate warming, it is possible that greater than at any other time during the last and reduce these functional effects of EDCs Climate Change (IPCC) 2001]. There appear endocrine variables influenced by POPs.
to be regional variations in climate change.
Important functions of THs are the regula- tion of metabolic processes and the growth periods of fasting as an adaptation to natural regions there has been a 10% decrease in snow and differentiation of tissues, including the seasonal reductions in food availability, and cover and ice extent since the late 1960s as a regulation of neuronal proliferation, cell THs seem to play an important role in regu- consequence of decreased diurnal temperature migration, and differentiation of the develop- lating these cycles. EDCs may disrupt the hor- ing animal (Zoeller et al. 2002). Sex steroid monal regulation and thus lead to suboptimal models predict that climate changes will be hormones are essential for reproduction, but timing of the fasting period. This scenario greatest at high latitudes (Phoenix and Lee they also are important in sexual behavior.
2004). Although we are only at an early stage Glucocorticosteroids are involved in a range VOLUME 114 | SUPPLEMENT 1 | April 2006 • Environmental Health Perspectives Endocrine-disrupting chemicals and Arctic climate change Conclusions
accumulated in seals from the coast of Hokkaido, Japan.
Karnovsky NJ, Kwasniewski S, Weslawski JM, Walkusz W, Climate change is likely to pose additional Environ Toxicol Chem 20:1092–1097.
Beszczynska-Moller A. 2003. Foraging behavior of little auks Colborn T. 2002. Preface. Environ Health Perspect 110(suppl 3):335.
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