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In: Endocrine Disrupters
T. Grotmol, A. Bernhoft, G.S. Eriksen and T.P. Flaten, eds.
Oslo: The Norwegian Academy of Science and Letters, 2006.
Effects of anthropogenic endocrine disrupters on
responses and adaptations to climate change*
Bjørn Munro Jenssen
Department of Biology, Norwegian University of Science and Technology,
NO-7491 Trondheim, Norway
E-mail: [email protected]
Telephone: +47 73 59 62 67
Telefax: +47 73 59 13 09
Abstract
The effects of global change on biodiversity and ecosystem functioning
encompass multiple complex dynamic processes, and climate change and
exposure to endocrine disrupting chemicals (EDCs) are currently regarded
as two of the most worrying anthropogenic threats to biodiversity and ecosystems. Various persistent organic pollutants (POPs), such as polychlorinated biphenyls (PCBs), dichlorodiphenyldichloroethylene (DDE), hexachlorobenzene (HCB) and oxychlordan, have been documented to affect
hormone homeostasis and function in laboratory and wildlife species. The
most pronounced effects have been reported on the thyroid hormone
system, but effects have also been reported on sex steroid hormones and
cortisol. Behavioural and morphological effects of POPs in marine mammals and seabirds are consistent with endocrine disruption. Since different
endocrine systems are important for producing adequate physiological and
behavioural responses to environmental stress, EDCs may interfere with
the adaptations to climate change. Such interacting effects can be expected
to be related to adaptive responses regulated by the thyroid, sex steroid and
glucocorticosteroid systems. There is concern for the possible effects that
EDCs may impose on the ability of animals to adapt to environmental
alterations caused by climate change.
* Part of this article is based on the paper: Jenssen BM. Endocrine-disrupting chemicals
and climate change: A worst-case combination for Arctic marine mammals and seabirds? Environ Health Perspect 2006; 114 (Suppl. 1): 76-80.
Introduction
Because of structural similarities with endogenous hormones, many anthropogenic (man-made) chemicals have the ability to mimic or block the effects of
endogenous hormones. Together with substances which may interfere with hormone metabolism, these chemicals may disrupt the normal actions of endogenous hormones and have thus become known as endocrine disrupting chemicals
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(EDCs) (1). Examples of environmental pollutants with endocrine disrupting
properties are certain pesticides, phtalates, alkylphenolic compounds, polychlorinated biphenyls (PCBs), polychlorinated dioxins and furans (PCDD/Fs),
bisphenol A, polybrominated diphenylethers (PBDEs), tetrabromobisphenol A
(TBBPA), and some heavy metals including lead, mercury, and cadmium (2,3).
Among the the environmental pollutants that are of most concern with respect
to their potency to act as EDCs, are some persistent organic pollutants (POPs).
POPs are chemicals that are resistant to physical, chemical and biochemical
degradation and therefore remain available for uptake and bioaccumulation for a
long period of time. POPs are also semi-volatile and are transported via the
athmospheric even to remote areas in the polar regions. Furthermore, POPs are
hydrophobic (albeit to differing degrees depending on their individual structures) and are therefore easily taken up by animals and bioaccumulated in fatty
tissues. Hence, POPs are present even in endemic Arctic species, such as polar
bears (Ursus maritimus) (4), glaucous gulls (Larus hyperboreus) (5), walrus
(Odobenus rosmarus) (6), ring seals (Phoca vitulina), bearded seals (Erignathus
barbatus) (7) and beluga whales (Delphinapterus leucas) (8).
Recently, polybrominated diphenylethers (PBDEs) and perfluorooctane sulfonate (PFOS) have also been reported in Arctic marine mammals and seabirds (912). The concentrations of some of these compounds, such as PBDEs show an
increasing trend in Arctic marine mammals (10). Thus, even though there is evidence that levels of classic POPs such as PCBs are decreasing or have levelled
off, such as reported in polar bears from the Svalbard and Barents Sea region
(13), it is likely that the total exposure of Arctic biota to POPs will increase
during the next decade.
It should also be noted that many animals, and in particular mammals and
birds, have the ability to biotransform many POPs into more polar metabolites
via the hepatic cytochrome P450 enzyme system or other phase I or II reactions.
Paradoxically, many of the metabolites formed during the phase I or phase II
metabolism have larger endocrine disrupting properties than their parent compounds (14). Thus, a well-developed detoxification system is not a guarantee
against endocrine disrupting effects of POPs.
Recently, climate change has been recognised as another significant threat
against Arctic biodiversity and ecosystem functioning. The Earth’s climate has
warmed by approximately 0.6 C over the past 100 years, and since 1976, the rate
has been greater than at any other time during the last 1000 years (15). Although
there is a debate about what are causative factors with respect to the climate
change issue, there is clear evidence of the ecological impacts of recent climate
change, from polar terrestrial to tropical marine environments (16-20). There
appears to be regional variations in climate change. For instance, as a consequence of decreased diurnal temperature ranges, in mid and high latitude regions
there has been a 10% decrease in snow cover and ice extent since the late 1960s
(15). General circulation models predict that climate changes will be greatest at
high latitudes (21).
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Since the bioaccumulation of many POPs is particularly high in marine endothermic animals (birds and mammals) (22), and since some of these animals also
have the ability to biotransform POPs into metabolites that may have even larger
endocrine disruptive capacities than their parent compounds, there are wellfounded reasons for being concerned about their effects on the hormonal balance
and function of these animals.
The thyroid hormone, sex hormone and glucocorticosteriod systems seem to
be among the most vulnerable endocrine systems with respect to disruption by
EDCs in endothermic animals. Important functions of THs are the regulation of
metabolic processes, growth and differentiation of tissues, including the regulation of neuronal proliferation, cell migration and differentiation of the
developing animal (23). Hypothyroidism may also affect behaviour and reduce
cognitive and learning abilities, affect motor coordination and cause menstrual
dysfunction and anovulation and infertility (24).
Sex steroid hormones are essential for reproduction, but do also play an
important role in sexual behavior. Glucocorticosteroids are involved in a range
of physiological processes, including reproduction, behavior and adaptation to
stress (25).
These three endocrine systems are important for animals to produce adequate
physiological and behavioural responses to environmental changes. There are
therefore good reasons for being particularly worried about the possibilities that
EDCs may affect endocrine processes involved in adaptations to climate change
in animals.
Because the climate change is predicted to be greatest at high latitudes (21),
there should be special concern for the possible effects that EDCs may impose
on the ability of Arctic marine mammals and seabirds to adapt to environmental
alterations caused by climate change (26). The aim of the present paper is therefore to give a short review of the effects of EDCs in Arctic mammals and
seabirds, and to assess the possible ecological outcome of interacting effects
between climate change and endocrine disrupters.
Endocrine disruption
Chemical pollutants have the ability to disrupt endocrine function in animal
groups ranging from planktonic invertebrates, amphibians and reptiles to birds
and large carnivorous mammals (27-30). Although most of the endocrine disrupting properties of chemicals have been documented through experimental exposure of animals, there is an increasing number of studies where disruptions or
alterations in reproductive activity, morphology or physiology have been reported in wildlife populations (28,30). The mechanisms by which the chemicals
exert their endocrine disruptive effects have been described in many of the
studies and reviews listed above, and will not be elucidated herein. In several
recent studies and reviews the link between endocrine disruption, particularly of
the thyroid system, and neurodevelopment and cognitive effects have received
attention (23,31-33).
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Effects on thyroid hormones
In captive harbour seals (Phoca vitulina), it has been shown that the response of
fasting on plasma total triiodothyronine (TT3) were lowered in seals fed herring
(Clupea harengus) from the Baltic Sea as compared to the control seals fed cleaner herring from the open waters of the Atlantic Ocean (34). In a similar feeding
experiment, captive harbour seals given a diet of organochlorine (OC) contaminated fish had significantly lower plasma levels of total thyroxine (TT4), free
thyroxine (FT4) and TT3 as compared to seals that were fed with less contaminated fish (35). Grey seal (Halichoerus grypus) pups from the highly polluted
Baltic Sea have been shown to have lower plasma concentrations of TT3 and
free triiodothyronine (FT3) compared to pups from the cleaner Norwegian Sea,
whereas there was no difference in plasma concentrations of TT4 and FT4
between the two groups (36). Since blubber concentrations of OCs were significantly higher in the Baltic group as compared to Norwegian group, the results
can be interpreted as a strong indication that plasma TT3 and FT3 concentrations may be susceptible to exposure to OCs in young phocids. Furthermore,
stranded immature northern elephant seals (Mirounga angustirostris) with a skin
diseases had elevated serum levels of PCBs, dichlorodiphenyltrichloroethane
(DDT) and DDE, and depressed levels of TT3 and TT4 as compared to healthy
controls (37). In northern fur seal (Callorhinus ursinus) neonates TT4 was reported to correlate negatively with several PCB-congeners (38).
In ribbon seals (Phoca fasicata) from Japanese waters, TT3 levels were
reported to decrease significantly with increased blubber concentrations of PCB170 and -180, whereas no such relationship was found between blubber PCBs
and FT3 (39). In Larga seals (Phoca largha), also from Japanese waters, plasma
TT3 and FT3 correlated negatively with blubber PCB concentrations, whereas
no such relationships were found between blubber PCB concentrations and TT4
and FT4 in neither Larga or ribbon seals (39).
There are reports of increasing levels of brominated flame retardants, such as
PBDEs, in Arctic ring seals (10), and in grey seals there are indications that
thyroid hormone levels may be affected by PBDEs (40).
The polar bear is the ultimate apex predator in the Arctic food chain. Even
though the polar bear has a relatively well developed capacity of metabolising
and excreting POPs (41), the polar bear accumulates relatively large amounts of
some POPs because they feed almost exclusively on large amounts of seal
blubber (42). During the last decades, Skaare and co-workers have conducted a
series of studies related to accumulation and effects of POPs in polar bears from
the Svalbard and the Barents Sea region. These studies have documented significant relationships between POPs and thyroid hormones and vitamin A (43). In
a recent study these relationships were studied in more detail, and it was found
that PCBs affected five thyroid hormone variables in females (TT4, FT4, FT3,
TT3:FT3, TT4:TT3) but only two variables in males (FT3, FT4:FT3) (44). This
indicates that female polar bears could be more susceptible to thyroid hormone
related effects of POPs than are males. The actions of thyroid hormones are
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mediated by nuclear thyroid hormone receptors that have their highest affinity
for FT3 (45). It is therefore worth noting that in polar bears PCB was reported to
affect T3 to a larger degree than T4 (44).
The glaucous gull is another top predator in the Arctic food web, and high
levels of POPs have been reported in this species (5,46). Verreault et al. (47)
reported significant negative relationships between plasma levels of hexachlorobenzene (HCB) and oxychlordane and plasma concentrations of FT4 and TT4 in
adult breeding glaucous gull males from Bear Island (Bjørnøya) in the Barents
Sea. Furthermore, negative correlations were found between several other OCs
and the FT4:FT3 and TT4:TT3 ratios in males. No effects were found in
females.
Reproductive hormones and stress hormones
In female polar bears plasma progesterone levels has been reported to be positively correlated with plasma concentrations of PCBs (48). In male polar bear
both plasma concentrations of OC pesticides and PCBs contributed negatively to
the plasma testosterone levels (49). Recently, relationships between blood levels
of OCs and cortisol levels have also been documented in polar bears from
Svalbard and the Barents Sea (50). The OC pesticides contributed negatively
whereas PCBs contributed positively to the variation in plasma cortisol. The
authors do however report that the overall contribution of the POPs to the
cortisol levels was negative.
Possible ecological effects of EDCs
In a series of papers Bustnes and co-workers have focused on ecological effects
of OCs in glaucous gulls from Bear Island. The proportion of time that adult
glaucous gulls were absent from the nest when not incubating and the total
number of absences, were both significantly related to blood concentrations of
PCBs (51). The authors suggested that the effect could be due to that individuals
with high blood concentrations of OCs need more time to gather food because of
either endocrine disruption or neurological disorders. Furthermore, females with
high blood levels of OCs, including HCB, oxychlordane, dichlorodiphenyldichloroethylene (DDE) and PCBs, were more likely to have non-viable eggs
than females with low blood OC levels (52). Adult yearly survival rate was also
reported to be significantly negatively related to blood concentrations of DDE,
persistent PCBs and HCB, and especially to oxychlordane (52).
Bustnes and co-workers also reported a significant positive relationship
between wing feather asymmetry (difference between the length of right and left
wing feathers) and blood concentrations of two PCB congeners (CB-99 and
-118), oxychlordane, DDE and especially HCB (53). Thyroid hormones are
central in regulating the moulting and replacement of feathers (54,55), and as
previously mentioned significant negative relationships between plasma concentrations of HCB and oxychlordan and thyroid hormones have been reported in
glaucous gulls (47). Thus, there may be a link between the thyroid hormone
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disruptive effects of HCB and oxychlordan and growth and development of the
primary wing feathers following moulting.
There is a high aerodynamic cost of asymmetry (56), and Bustnes et al. (51)
suggested that increased flight costs may be an important factor in explaining
why birds with high blood concentrations of POPs spend more time on feeding
trips than birds with low levels. Exposure to PCBs has been associated with
cognitive and behavioral changes (57-59), and it has been suggested that the
effects of PCBs on brain development may be attributable, at least in part, to
their ability to affect the thyroid system (23,60). It is therefore tempting to
speculate that thyroid hormone disruption caused by POPs may be the ultimate
cause of this altered parental behavior. However, more research into linking
endocrine disruption and behavioral and ecological alterations in free-living
animals is needed before conclusions on this aspect can be drawn.
It has been reported that climatic warming may make birds breed earlier (61).
Negative relationships between sea temperature and hatching date has been
reported for several seabird species (62-64). On the other hand, Helberg et al.
(65) reported significant positive relationships between blood concentrations of
OCs, and in particular HCB and DDE and egglaying date in female black
backed-gulls (Larus marinus). Thus, females with high burdens of OCs breed
later than less contaminated individuals. Since both thyroid and sex hormones
are important determinants for the timing of egglaying, it is possible that
disruption of the thyroid and sex hormone balance caused by OCs could be
linked to delayed egglaying. Based on the results from this study (65) it can be
hypothesised that OCs may counteract the apparent adaptive response of
seabirds to breed earlier as the environmental temperature rises due to climatic
warming. In the Arctic the summer season is short, and a proper timing of
breeding, moulting and migration is important for seabirds. Exposure to EDCs
could disrupt the endocrine systems and mechanisms that regulate these events,
leading to a sub-optimal timing in relation to the season.
In polar bears, learning and cognitive abilities are probably important factors
for successful hunting. There is concern that disruption of the thyroid hormone
balance caused by EDCs may effect neurodevelopment, and that this in turn may
affect behavior and cognitive abilities of wildlife (66). Since maternal hypothyroidism is linked to disorders of the neurophysiological development in the
offspring (67), cubs of polar bear females with lowered thyroid hormone levels
due to exposure to anthropogenic chemicals may suffer from such disorders. It
should, however, be noted that because information on normal baseline levels of
thyroid hormones in polar bears is lacking, it is not known if the polar bear
females with high PCB levels and low thyroid hormone levels (44) suffer from
hypothyroidsm. However, it can hypothesised that PCBs and other anthropogenic chemicals that affect thyroid hormone balance may disrupt behaviour and
cognitive abilities in polar bears, and that this may have a negative effect on
their hunting success and their abilities to cope with changes in prey distribution
caused by climate change induced reductions of ice-coverage. In the case of a
temporal and/or spatial change in the distribution of food caused by climate
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change, an altered behavior caused by EDCs or an reduced ability to respond
adequately to such major changes could hamper reproductive success and even
survival rates of adult animals.
The increased levels of progesterone reported in polar bears (48) may disturb
the normal reproductive cycle of the females and thus hinder successful mating.
In male polar bear both plasma concentrations of OC pesticides and PCBs contributed negatively to the plasma testosterone levels (49), and it is thus possible
that male reproductive performance may be affected by POPs.
Furthermore, it is possible also that the negative effects of POPs on plasma
cortisol levels reported in polar bears from Svalbard and the Barents Sea (50)
may interfere with physiological processes and render the polar bears less able
to deal with other environmental stressors, such as those caused by climatic
warming.
Ecological studies of the Svalbard population of polar bears have shown that
there are indications of reproductive impairment of females, lower survival rates
of cubs or increased mortality of reproductive females, and it has been suggested
that these may be contaminant-related (68). Although it is difficult to prove any
clear cause-effect relationships, it is possible that endocrine disrupting properties
of many POPs could contribute to such population effects.
Many Arctic marine mammals undergo periods of fasting, mainly due to
natural seasonal reductions in food availability, and thyroid hormones seem to
play an important role in regulating these cycles. As previously reported in
fasting harbour seals, EDCs may disrupt the thyroid hormone homeostasis (34),
which possibly may lead to a sub-optimal timing of the fasting period.
Conclusions
Climate change is likely to pose additional stress to individuals, and since different endocrine systems are important for adequate physiological and behavioural
responses to environmental stress, EDCs may interefere with the adaptations to
the increased stress situation. Thus, when taking into consideration the longrange transport of EDCs into the Arctic ecosystem, the combination of EDCs
and climate change may be a worst case scenario for Arctic mammals and seabirds. However, the knowledge of the responses of animals to multiple natural
and anthropogenic stressors is at present time not sufficient to forecast the
combined effects of these two stressors, and there is a clear need for more focus
on the interacting effects of multiple stressors (natural or anthropogenic) on
wildlife.
Acknowledgements
This publication was financed by the Norwegian Research Council project no. 155933/S30.
The author has no competing financial interests. I also wish to thank colleagues and my past
and present students for co-operation and fruitful discussions on the issue of effects of
anthropogenic pollutants on wildlife.
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