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: [email protected]
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,
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
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VOLUME 114 | SUPPLEMENT 1 | April 2006 • Environmental Health Perspectives
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Fachbeitrag Dr. Möbius I. Teil Literaturverzeichnis ANDRIAN, E., GRENIER, D., ROUABHIA, M.: In vitro models of tissue penetration and destruction by Porphyromonas gingivalis. Infect Immun. 72, 4689-4698 (2004) BACHMANN, A.: Der Biofilm ist nur zu managen – die Entfernung ist nicht möglich und nicht sinnvoll. DZW 9, 28-29 (2005) FILOCHE, SK., ZHU, M., WU, CD.: In situ biofilm formati