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First published online December 1, 2006
Journal of Experimental Biology 209, 4957-4965 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02610
Corticosterone selectively decreases humoral immunity in female eiders during incubation
Institut Pluridisciplinaire Hubert Curien (IPHC), Département Ecologie, Physiologie et Ethologie (DEPE), UMR 7178 CNRS-ULP, 23 rue Becquerel, F-67087 Strasbourg Cedex 2, France
* Author for correspondence (e-mail: sophie.bourgeon{at}c-strasbourg.fr)
Accepted 23 October 2006
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Key words: bird, body reserve, fasting, glucocorticoid, immunosuppression
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Introduction |
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; Stearns,
1992). This concept is based on physiological trade-offs between
resource-demanding activities within an individual. Recently, the costs of
immune defenses have been emphasized
(Gustafsson et al., 1994;
Sheldon and Verhulst, 1996;
Råberg et al., 1998).
Namely, parental effort may induce immunosuppression in birds
(Moreno et al., 1999).
Acquired immunity can be classified into humoral immunity (mediated by
B-lymphocytes) and cell-mediated immunity (mediated by T-lymphocytes)
(Roitt et al., 1998).
Deerenberg et al. (1997) showed
in captive zebra finches Taeniopygia guttata that their humoral
immunity was progressively reduced when the reproductive effort is increased.
Similarly, when raising experimentally enlarged broods, female pied
flycatchers Ficedula hypoleuca exhibited reduced T-cell-mediated
responses (Moreno et al.,
1999). Previous studies have shown that the acquired immunity of
female common eiders Somateria mollissima is suppressed during the
incubation fast (Hanssen et al.,
2004; Bourgeon et al.,
2006), while its experimental activation has strong negative
effects on the fitness of female eiders
(Hanssen et al., 2004).
Whatever the ultimate factors explaining such an immunosuppression in breeding
eider ducks, the underlying physiological mechanisms still remain unknown.
Among potential proximate factors underlying immunosuppression during
reproduction, a link between immunocompetence and hormonal changes has been
proposed (see Deerenberg et al.,
1997).
Glucocorticoids are an essential component of the endogenous
immunoregulatory network, while also being associated with stress. Hence,
these hormones establish a close endocrine link between immunocompetence and
stress (Apanius, 1998).
Råberg et al. (Råberg et al.,
1998) hypothesized that corticosterone, secreted during stressful
activities, reduces the acquired immune function. However, while the
T-cell-mediated immune response was suppressed by experimentally elevated
corticosterone levels in nonbreeding New Jersey house sparrows Passer
domesticus (Martin II et al.,
2005), it did not significantly covary with natural corticosterone
concentrations in breeding barn swallows Hirundo rustica
(Saino et al., 2002).
Similarly in female common eiders both components of the acquired immunity
decreased independently of plasma corticosterone level, which itself did not
vary significantly over the incubation period
(Bourgeon et al., 2006).
However, in several bird species, organisms are metabolically prepared for a
longterm fast (Le Maho et al.,
1981; Cherel et al.,
1988; Lindgård et al.,
1992). Indeed, fasting is first characterized by exhaustion of
glycogen reserves (phase I) before a long period of protein sparing and
preferential mobilization of fat stores (phase II), which is followed by a
period of increased net protein catabolism (phase III). While phases I/II are
characterized by the maintenance of low plasma levels of corticosterone, phase
III of fasting is associated with an increase in plasma corticosterone levels.
Such an elevation could be responsible for the increase in protein catabolism
(proteolysis), because corticosterone is known to mobilize peripheral calorie
stores for glucose production and energy utilization
(Robin et al., 1998).
Depending on conditions during the breeding season, incubating female eiders
can enter phase III of fasting (see Le
Maho, 1981; Le Maho et al., 1983).
Our main objective in this study was to examine the effects of increased plasma corticosterone levels on both components of the acquired immunity in wild female common eiders at different stages of their incubation fast. To this end, female eiders, nesting in the high Arctic, were implanted with corticosterone pellets both at the beginning and at the end of incubation. Subsequently, female total immunoglobulin levels, T-cell-mediated immune response, body mass and plasma corticosterone levels were measured and compared with those in control birds prior to and after manipulation. To mimic corticosterone effects on body mass, fasting duration in a group of females (termed `late fasters') was experimentally extended. Body mass loss in these females was therefore increased, while corticosterone levels remained unaltered (birds remained in phase II and did not reach phase III). This allowed us to discriminate the effects of increased body mass loss on the acquired immunity from those of elevated corticosterone levels. We predicted that an increased plasma corticosterone level, which increases proteolysis during the female fast, should have immunosuppressive effects. Implanted females should therefore show T-cell-mediated immune responses and/or an immunoglobulin level lower than in control females but similar to that of `late fasters'.
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Materials and methods |
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). All birds started their incubation between June 07 and June
15, the main laying period for the colony. Ducks that laid their eggs after
this period were not considered in this study. Ambient temperatures in June
and July ranged from 2 to 10°C.
Sampling protocol
Nests were checked at least every second day throughout the study period.
This was done to determine initial clutch size but also to investigate the
rate of egg predation and nest desertion. A clutch of eggs was considered
complete when no additional egg was laid during a 2-day period
(Yoccoz et al., 2002). Females
that suffered partial egg predation were excluded from this study. Female
eiders were caught on their nests using a bamboo pole with a nylon snare.
Blood was collected from the brachial vein within 3 min of capture, stored in
tubes containing EDTA (an anticoagulant agent) and kept on ice until being
centrifuged in the laboratory (at 4472 g), for 5 min, at
4°C). Plasma samples were stored at -20°C and subsequently used to
measure immunoglobulin and corticosterone levels. After blood sampling, body
size was recorded (wing and tarsus lengths) and birds were weighed using a
portable electronic balance (to ±2 g).
Experimental groups and corticosterone implantation
A total of 36 females with mean clutch sizes of 3-4 eggs (3.69±0.08
eggs, N=36) (mean ± s.e.m.) was used in this study. Freely
incubating females were classified into two experimental groups:
corticosterone (N=18) and control females (N=18). Previous
results have shown that both components of the acquired immune system are
decreased during incubation in eider ducks
(Bourgeon et al., 2006), so
females from both groups were caught during the first part of incubation
(10.64±0.62 days, N=22) (mean ± s.e.m.) (11 females
from each group) and near the end of incubation (20.07±0.24 days,
N=14) (7 females from each group). After capture, a blood sample was
taken, and body size and mass were recorded. Half of the females were then
implanted with corticosterone pellets (see below), while the others underwent
the same procedure without actual implantation. Birds were held in cages for
the following 5 days at ambient temperatures, with snow given as fresh water
ad libitum. Four days after the treatment (18.31±0.87 days
into their incubation, N=36) (mean ± s.e.m.), another blood
sample was taken, a phytohemagglutinin (PHA) skin test conducted (see below),
and body mass determined. Birds were released 24 h later, after the PHA skin
test had been read. Additionally, in a group termed `late fasters', which
consisted of seven captive females with mean clutch sizes from 2-5 eggs
(3.43±0.53 eggs, N=7) (mean ± s.e.m.), fasting duration
was experimentally extended. Birds remained in phase II of fasting during
experimentation and never entered into phase III. This protocol allowed
discrimination of the effects of increased body mass loss on the acquired
immunity from those of elevated corticosterone levels. To this end, these
females had been incubating eggs for at least 23 days (24.86±0.40 days,
N=7) (mean ± s.e.m.), i.e. eggs were close to hatching. We
took a blood sample and recorded body size and mass. Females were then held in
captivity for 5 days (29.86±0.40 days into their incubation,
N=7) (mean ± s.e.m.), at which point a further blood sample
was taken, a PHA skin test performed (see below), and body mass recorded.
Females were released 24 h after this, when the PHA skin test had been
read.
Corticosterone pellets (100 mg, 21 day release, G-111) were obtained from Innovative Research of America (Sarasota, FL, USA). The implants slowly release the hormone, which enters the bloodstream. In preliminary trials we found that this dose was sufficient to induce marked increases in the level of plasma corticosterone and accelerate body mass loss as early as 2 days after the start of treatment (S.B. and T.R., unpublished data). For the implantation of the corticosterone pellets we followed the recommendations of the manufacturer. Briefly, a small patch of skin at the back side of the bird's neck was shaved and disinfected using alcohol and betadine (iodine solution). A small incision equal to the size of the pellet was made and the implant was inserted underneath the skin. The skin was closed with a single stitch, using surgical thread. The wound was cleaned with betadine and sprayed with an aluminium powder. The surgical procedure required less than 10 min. Control animals underwent the identical procedure, without actual insertion of a pellet.
T-cell-mediated immune response: PHA skin test
For this test we challenged one wing-web with the mitogenic PHA, while the
other wing-web (control) was injected with phosphate buffered saline (PBS).
Briefly, 100 µl of 5 mg ml-1 PHA (Sigma L 8754) in PBS were
injected intradermally into the right wing-web, while the left wing-web was
injected with an equal volume of PBS. This procedure was shown to induce
little physiological stress in birds
(Merino et al., 1999).
Injection sites on the wing-web were measured using a micrometer calliper
(three readings) just before and 24 h after injection with PHA or PBS. The
T-cell-mediated immune response was taken as the difference between the two
wing-web swellings.
Immunoglobulin levels: ELISA test
A sensitive ELISA method was used to determine the amount of serum
immunoglobulins in eider duck blood. This method using commercial anti-chicken
antibodies has so far been validated in six wild avian species
(Martinez et al., 2003).
Despite the fact that Anseriforms have an additional immunoglobulin isotype
(IgY), which is not found in other birds
(Parham, 1995), we assumed
linear cross-reactivity. Accordingly, the values obtained were used as
relative immunoglobulin levels.
To determine the linear range of the sigmoid curve, ELISA plates were coated with serial dilutions of serum (100 µl) in carbonate-bicarbonate buffer (0.1 mol l-1, pH 9.6) and incubated overnight at 4°C. We selected the data obtained from trials using the serum dilution nearest to the centre of its linear range. ELISA plates were then coated with 100 µl of diluted serum samples from female eiders (two samples per female diluted to 1/32 000 in carbonate-bicarbonate buffer) and incubated for 1 h at 37°C. After a second incubation overnight at 4°C, the plates were washed with a solution (200 µl) of phosphate buffer saline and Tween (PBS-Tween), and a diluent (100 µl), containing 5% powdered milk in PBS was added. Following incubation for 1 h at 37°C, the plates were washed with PBS-Tween buffer. 100 µl of anti-chicken conjugate (Sigma A 9046) was added at 1:250 (v/v) and the plates were incubated for 2 h at 37°C. After three washes, the plates were filled with 100 µl of a solution consisting of 2,2'-azino-bis-(3-ethylbenzthiazoline-6-sulphonic acid (ABTS) and concentrated hydrogen peroxide diluted to 1:1000. Following incubation for 1 h at 37°C, absorbance was measured at 405 nm using a plate spectrophotometer (Awareness Technology, Inc., Palm City, FL, USA).
Assessment of the corticosterone levels
Corticosterone concentrations were determined by radioimmunoassay (RIA) in
our laboratory using an 125I RIA double antibody kit from ICN
Biomedicals (Costa Mesa, CA, USA). The corticosterone RIA had an intra-assay
variability of 7.1% (N=10 duplicates) and an inter-assay variability
of 6.5% (N=15 duplicates).
Statistical analysis
Statistical analysis was conducted with SPSS 12.0.1 (SPSS Inc., Chicago,
IL, USA). Values are means ± standard error (s.e.m.). Corticosterone
levels were not normally distributed (Kolmogorov-Smirnov test,
P<0.05). Hence, data were log transformed to meet parametric
assumptions, before parametric tests were used. Repeated measures (RM) two-way
ANOVA was used to test for the effects of the treatment and incubation stage
on corticosterone levels, body mass and immunoglobulin level. Two-way ANOVA
was used to test for the effects of the treatment and incubation stage on the
T-cell-mediated immune response. Linear regression analysis was used to assess
the relationships between all parameters measured.
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Effects of corticosterone implants on body mass
As expected, implants induced a significant increase in corticosterone
levels (RM two-way ANOVA: effects of repetition:
F1,32=65.95, P<0.0001; effects of treatment:
F1,32=54.16, P<0.0001; effects of incubation
stage: F1,32=0.06, P=0.81; interaction:
F1,32=0.73, P=0.40). Four days after
implantation, corticosterone levels in implanted birds were 6 times higher
than in control females, independent of incubation stage. Moreover,
corticosterone levels in `late fasters' were far below the levels of implanted
females. In fact, they were not significantly different from the levels in
control females sampled at the end of their incubation period
(T-test: t=-0.03; N=25; P=0.97). Body mass
in corticosterone implanted females was significantly decreased by 18%, while
it only decreased by 12% in control females (RM two-way ANOVA: effects of
repetition: F1,32=1191.35, P<0.0001; effects
of treatment: F1,32=30.46, P<0.0001; effects
of incubation stage: F1,32=0.10, P=0.33;
interaction: F1,32=0.78, P=0.38). Four days after
implantation, implanted females were significantly lighter than control
females (by 8%), independent of the incubation stage. In fact, body mass loss
per day in implanted females was 35% higher than in control females,
regardless of the incubation stage (two-way ANOVA: effects of treatment:
F1,32=25.89, P<0.0001; effects of incubation
stage: F1,32=1.29, P=0.26; interaction:
F1,32=0.01, P=0.92). Corticosterone levels in
birds during early incubation were negatively related to body mass only after
the implantation (Table 3),
when high corticosterone levels were associated with low body mass values.
However, there was no significant relationship between these parameters in
birds near the end of their incubation period, neither before nor after
implantation (Table 4).
Finally, body mass of `late fasters' was not significantly different from that
of implanted females but was significantly lower than in control females
sampled at the end of their incubation (8%;
Table 2) (RM one-way ANOVA:
effects of repetition: F1,18=707.63, P<0.0001;
effects of treatment: F2,18=10.89, P=0.001).
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Effects of corticosterone on the T-cell-mediated immune response and immunoglobulin level
Corticosterone implants had no significant effect on the T-cell-mediated
immune response (two-way ANOVA: effects of treatment:
F1,32=2.49, P=0.12; effects of incubation stage:
F1,32=2.94, P=0.10; interaction:
F1,32=0.003, P=0.95;
Fig. 1). Responses in implanted
females were similar to that of control females, independent of the incubation
stage. However, the immune response in `late fasters' was significantly
reduced when compared with implanted and control females at the end of their
incubation (53% and 63%, respectively) (one-way ANOVA: effects of treatment:
F2,18=9.39, P=0.002;
Fig. 1). There was no
relationship between the T-cell-mediated immune response and plasma
corticosterone levels at any stage (Tables
3 and
4). However, there was a
positive significant relationship between the T-cell-mediated immune response
and body mass but only during early incubation (Tables
3 and
4), so that the immune response
was stronger in heavier females.
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;
Bourgeon et al., 2006). Among
other potential scenarios, reduced immunocompetence during reproduction has
been attributed to hormonal regulation, in particular through the action of
glucocorticoids (Deerenberg et al.,
1997; Råberg et al.,
1998). Hence, the main objective of the current study was to
investigate the potential physiological mechanisms underlying such
immunosuppression. We therefore assessed the effects of exogenous
corticosterone on both components of the acquired immune system in female
eiders during different stages of their incubation fast. In addition, a group
of females whose fasting duration was experimentally extended was used to
discriminate the effects of increased body mass loss on the acquired immunity
from those of elevated corticosterone levels. Experimentally increased plasma corticosterone levels only affected one of the two components of the acquired immunity. The immunoglobulin level in implanted females was significantly decreased when compared with that of control females. This response was strongest when birds were implanted at the beginning of their incubation fast. However, the T-cell-mediated immune response was not significantly affected by the treatment. Paradoxically, there was no significant relationship between plasma corticosterone and immunoglobulin levels after the implantation at any incubation stage. By contrast, before the treatment in ducks that were near the end of their incubation, high corticosterone levels seemed to be associated with a low immunoglobulin level.
Whatever the effects of exogenous corticosterone, and similar to an earlier
investigation (Bourgeon et al.,
2006), we did not find a significant relationship between both
components of the acquired immunity. This lends support to the view that
variations in one component of the acquired immunity are not necessarily a
reliable indicator of changes in the other
(Norris and Evans, 2000). In
fact, in the present study, the immunoglobulin level seemed to be more
sensitive to corticosterone treatment than the T-cell-mediated immune
response. In control females, the immunoglobulin level significantly decreased
throughout incubation, while the T-cell-mediated immune response did not vary
significantly. This would seem to contrast with the finding of a previous
investigation (Bourgeon et al.,
2006) suggesting that both components significantly decrease
throughout the incubation fast of eider ducks. This apparent discrepancy could
lie in the fact that smaller sample sizes have been used, which is reinforced
by high variances observed in this immune response. Moreover, we cannot
exclude the possibility that effects of corticosterone on the T-cell-mediated
immune response might require more time (see
Dhabhar and McEwen, 1997)
and/or higher corticosterone concentrations. In the current study, a
significant decrease in the T-cell-mediated immune response was only observed
in `late fasters', while their immunoglobulin level was not lower than that of
corticosterone implanted or control females. Implanted females significantly
lost more weight than control females, which is consistent with the
observation (Cherel et al.,
1988) that high levels of corticosterone increase proteolysis in
fasting birds. In a preliminary study on captive female eiders, high doses of
exogenous corticosterone, administered for a few days, induced a rise in
plasma levels of uric acid, indicating protein breakdown
(Criscuolo et al., 2005).
Corticosterone levels of `late fasters' in the current study were similar to
that of control females but body mass was 8% lower in the former. Hence, the
T-cell-mediated immune response appears to be more sensitive to body mass loss
than to elevated levels of corticosterone, supporting the view of an indirect
effect of corticosterone on this immune parameter. Accordingly, in the present
study we found a positive relationship between body mass and T-cell-mediated
immune response, where the response was stronger in females with a greater
body mass. By contrast, the immunoglobulin level appears to be more sensitive
to high corticosterone levels than to body mass loss. Nevertheless,
corticosterone levels and body mass were negatively related in the current
study, so that high levels of corticosterone were associated with low body
mass. Our results agree with previous findings from breeding black-legged
kittiwakes Rissa tridactyla, where high corticosterone levels were
associated with a marked decline in body condition
(Kitaysky et al., 1999). In
this context, it would be interesting for future studies (1) to experimentally
extend the fasting duration of eiders until they reach phase III of fasting or
(2) to find free-ranging birds that spontaneously shift from lipid to protein
utilization, so that the effects of both elevated corticosterone levels and
decreased body mass on the acquired immunity can be examined.
The present study showed that an increasing body mass loss, caused either
by corticosterone administration, or by an experimental extension of fasting
duration, negatively affected the birds' immunoglobulin level and their
T-cell-mediated immune response, respectively. This result lends support to
the resource-limitation hypothesis, which predicts that investment in costly
behaviours, such as reproduction, reduces the amount of resources available to
other systems, such as the immune system
(Sheldon and Verhulst, 1996;
Råberg et al., 1998).
However, evidence for an energetically costly immune response is still
equivocal (Råberg et al.,
1998; Eraud et al.,
2005; Verhulst et al.,
2005). Whatever the ultimate factors explaining immunosuppression
during reproduction, corticosterone was proposed to regulate immunosuppression
in incubating birds (Deerenberg et al.,
1997; Råberg et al.,
1998; Saino et al.,
2003). However, during fasting corticosterone should be maintained
at low levels to avoid metabolic disorders, such as protein catabolism
(Cherel et al., 1988). In the
present study we did not find marked variations in corticosterone levels
during the incubation period of control and `late fasting' females. However,
`late fasters' had a lower T-cell-mediated immune responses than
corticosterone implanted or control females. This would support the view that
fasting duration and/or body composition (see below) might be relevant
parameters for immunosuppression.
Other aspects of immunosuppression, namely humoral immunity, could be
mediated by factors related to fuel utilization or body mass loss. Such a
relationship between energy storage/mobilization and immunocompetence might
plausibly be mediated through nutritional and/or endocrine factors
(Apanius, 1998). Exogenous
administration of corticosterone is likely to increase proteolysis.
Consequently, lean body mass will be decreased, while the energy stored as
lipids within the body will be spared. Hence, for the same final body mass,
adiposity of `late fasters' should be lower than for corticosterone implanted
females, as reported to be the case in dark-eyed juncos Junco
hyemalis treated with corticosterone
(Gray et al., 1990).
Currently, adipose tissue is perceived as an active participant in the
regulation of essential and prominent body processes such as immune
homeostasis (Matarese and La Cava,
2004). This raises the question of how body reserves might control
the immune system (Demas and Sakaria,
2005). Some adipose humoral signals, such as leptin, are generated
in proportion to fat stores and act on feedback control systems to influence
numerous biological processes
(Lõhmus and Sundtröm,
2004; Matarese et al.,
2005). In fact, leptin is secreted primarily by adipose tissue and
has been shown to enhance a variety of immunological parameters in mammals
(Lord et al., 1998;
Faggioni et al., 2001;
Demas et al., 2003) and birds
(Lõhmus et al., 2004).
Consequently, leptin levels might be lower in `late fasters' when compared
with corticosterone implanted eiders. To gain further insight into the role
that leptin plays for the immune system of fasting birds, plasma measurements
of leptin and manipulation of its circulating concentrations would be
useful.
In conclusion, exogenous corticosterone decreased only one component of the
acquired immune system in incubating female eider ducks. While the treatment
significantly decreased their immunoglobulin level, their T-cell-mediated
immune response was not affected. Implanted females lost significantly more
weight than control birds. Females, whose fasting duration was experimentally
extended, increasing body mass loss, displayed lower T-cell-mediated immune
responses than implanted females, while their corticosterone levels remained
at baseline values. Consequently, the immunosuppressive effect of
corticosterone appears to be mediated by its effect on body reserves, which
have been shown to play an important role in the regulation of the immune
system. For example, leptin, which conveys information on energy availability,
could be involved in the observed immunosuppression. Further experiments are
required to determine the relationship between body condition and immune
function in incubating female eiders. Our results raise the question of the
physiological mechanisms that can explain the effects of corticosterone on the
immune response. Furthermore, could it be that depending on its concentration,
this hormone is able to trigger different responses, as has already been
reported in the context of foraging behaviour
(Wingfield et al., 1998).
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