Behavioural and neuroendocrine effects of environmental background colour and social interaction in Arctic charr (Salvelinus alpinus)
1 Evolutionary Biology Centre, Department of Limnology, Uppsala University,
Norbyvägen 20, SE-752 36 Uppsala, Sweden
2 Department of Animal Physiology, Faculty of Science, University of
Nijmegen, Toernooiveld 1, 6526 ED Nijmegen, The Netherlands
3 Evolutionary Biology Centre, Department of Animal Development and
Genetics, Uppsala University, Norbyvägen 18A, SE-752 36 Uppsala,
Sweden
4 Evolutionary Biology Centre, Department of Comparative Physiology, Uppsala
University, Norbyvägen 18A, SE-75236 Uppsala, Sweden
* Author for correspondence (e-mail: svante.winberg{at}ebc.uu.se )
Accepted 23 May 2002
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Summary |
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Key words: Salmonidae, serotonin, dopamine, norepinephrine, pro-opiomelanocortin-derived peptide, skin darkening, brain, social signal, Arctic charr, Salvelinus alpinus
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Introduction |
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In socially organised teleosts, as in many other vertebrates, subordinate
individuals are subjected to chronic stress induced by a general lack of
control, as well as by direct aggressive acts from individuals of higher
social rank (Winberg and Lepage,
1998). Sustained social stress leads to chronic activation of the
hypothalamicpituitaryinterrenal (HPI) axis, the teleost
homologue of the mammalian hypothalamicpituitaryadrenal (HPA)
axis (Winberg and Lepage,
1998
; Øverli et al.,
1999
; Höglund et al.,
2000
). Alpha-melanocyte-stimulating hormone (
-MSH) and
adrenocorticotrophic hormone (ACTH), two hormones involved in the control of
interrenal cortisol release (Balm et al.,
1995
), also have the ability to induce skin darkening
(Fujii and Oshima, 1986
).
Brain monoamines are important in the control of pituitary release of
-MSH and ACTH (Höglund et al.,
2000
; Bentley,
1998
). Serotonin (5-hydroxytrypamine, 5-HT) stimulates the release
of
-MSH in mammals (Carr et al.,
1991
), and Olivereau et al.
(1980
) obtained results
suggesting that 5-HT might serve a similar function in teleosts. Moreover,
5-HT seems to stimulate the HPA axis in mammals
(Dinan, 1996
) and 5-HT has
also been reported to stimulate HPI axis activity in rainbow trout
(Oncorhynchus mykiss) (Winberg et
al., 1997
). In addition, the behavioural suppression observed in
socially subordinate fish is an effect that, at least in part, appears to be
mediated by a stress-induced activation of the central 5-HT system
(Winberg and Nilsson, 1993
;
Øverli et al., 1998
).
By contrast, the brain catecholamines dopamine and norepinephrine exert
inhibitory effects on the release of
-MSH from the pituitary
(Bentley, 1998
), and these
neurotransmitter systems also appear to facilitate intraspecific aggressive
behaviour, thus having effects opposing those of 5-HT on both behaviour and
skin colour (reviewed by Winberg and
Nilsson, 1993
).
Social subordination results in an elevation of plasma -MSH levels
and skin darkening in juvenile Arctic charr (Salvelinus alpinus)
interacting in small groups on a pale background
(Höglund et al., 2000
).
If skin darkening in subordinate Arctic charr acts as a signal announcing
submissive behaviour, it is possible that environmental background colour,
through its effect on body pigmentation, might affect agonistic behaviour in
socially interacting fish.
The aim of the present study was to investigate the effect of environmental background colour on socially induced skin darkening and aggressive behaviour in juvenile Arctic charr.
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Materials and methods |
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Behavioural observations
Behavioural observations were performed in six glass aquaria (1000
mmx300 mmx500 mm) continuously supplied with aerated tap water (1
l min-1, 10-12°C). Each aquarium was divided into four 25 l
chambers by removable black plastic walls. Half of these chambers had a white
base and back, whereas the other half had a black base and back. Since the
removable plastic walls, and tank ends, were black in all cases, the fish on
white backgrounds still experienced black lateral sides. Light was provided by
two 20 W fluorescent tubes (warm white) placed 250 mm above the water surface.
At the start of the experiment, fish were transferred from the holding tank
and tagged by small clips in the caudal fin, before being isolated in
individual chambers within the observation aquaria. The fish were kept
visually isolated for 3 weeks before the experiment to reduce the effects of
previous tank colour and social experience. After the isolation period,
size-matched pairs (within-pair body mass deviation <5%, based on mass
determined prior to acclimation), consisting of fish that had been isolated on
the same background colour, were formed by gently removing the plastic walls
that had kept them separated. Experimental fish were allowed to interact in
pairs for 5 days. Eight fish on white and eight fish on black background
colour were kept visually isolated throughout the experiment and served as
controls.
The fish were hand-fed commercial trout pellets (Ewos, ST40) daily at 15:00 h to satiation during the isolation period as well as while interacting in pairs, except on the day of sampling when the fish were not fed.
Aggressive acts performed and received by individual fish were counted during two daily observation sessions of 5 min each, at 10:00 h and 16:00 h. Three types of aggressive acts were registered: attack, charge and bite. The fish were observed through the front of the aquaria by an observer who was not screened from the fish but remained motionless during the observation session. To reduce further the disturbance of the fish during behavioural observations, light was kept low in the room. The first observation was performed 30 min after pairing of the fish and the last on day 4, the day before terminating the experiment. Since the number of experimental aquaria was limited, the experiment was performed in two consecutive rounds, the second following immediately after the first. The first round consisted of four controls (two on black and two on white backgrounds) and 10 pairs of socially interacting fish (five pairs on black backgrounds and five on white backgrounds) and the second round of 12 controls (six on black and six on white backgrounds) and six pairs of socially interacting pairs (three on black and three on white backgrounds).
In one pair of fish kept on a black background, no aggressive acts were observed and in one pair on a white background the subordinate died. These two pairs were excluded from analysis of skin colour, hormones and brain monoamine levels.
Skin pigmentation measurements, and blood and brain tissue
sampling
Skin pigmentation, quantified as the darkness of the skin, was measured by
an image-analysing system described by Höglund et al.
(2000), 24 h prior to and on
day 5 of social interaction. In short, skin pigmentation was measured by
placing the fish in a plastic box with a transparent cover. The box was
stuffed with foam rubber, which immobilised the fish against the transparent
cover. The fish was filmed with a ccd-video camera through the plastic cover
under constant light conditions. Thereafter, the filmed fish was analysed by
an image analysis program (Scion Image, based on NIH image for Macintosh
modified for windows, by Wayne Rasband, NIH, Betheseda, MD, USA). Skin
darkness was measured on a linear black-white scale where 0 corresponded to
white and 255 to black. A grey-scale with eleven standard measure points
ranging from 0 to 250 and a step value of 25 was attached to the transparent
cover and used for calibration between measurements. The time for the pigment
measuring procedure, from netting to the completion of measuring, was
approximately 40 s. Immediately after the second skin pigmentation
measurement, the fish were anaesthetised (500 mg l-1
ethyl-m-aminobenzoate methanesulphonate) and blood (approximately 1
ml) was collected from the caudal vasculature, using a syringe pre-treated
with 1.5 mg of EDTA. Blood samples were rapidly transferred to Eppendorf tubes
containing aprotinin (Sigma, A1153, 1 mg ml-1 blood) and were
centrifuged at 1500 g for 10 min at 4°C. Following
centrifugation, the blood plasma was removed, divided into samples, frozen on
dry ice and stored at -80 °C. Following blood sampling, the fish were
killed by decapitation, and the brain was rapidly removed (within 2 min) and
divided into telencephalon (excluding olfactory bulbs), hypothalamus
(excluding the pituitary gland), optic tectum and brain stem (including the
medulla and part of the spinal cord). Each brain division was wrapped in
aluminium foil, frozen in liquid nitrogen and stored at -80°C.
Measurements of skin pigmentation and sampling of blood and brain tissue was
always performed between 10:00 and 12:00 h.
Assays
The frozen brain samples were homogenised in 4 % (w/v) ice-cold perchloric
acid containing 0.2 % EDTA and 40 ng ml-1 epinine
(deoxyepinephrine, the internal standard), using a PotterElvehjem
homogenizer (optic lobes, cerebellum and brain stem) or an MSE 100 W
ultrasonic disintegrator (telencephalon and hypothalamus).
5-HT, 5-hydroxyindoleacetic acid (5-HIAA), dopamine,
3,4-dihydroxyphenylacetic acid (DOPAC, a major dopamine metabolite),
norepinephrine and 3-methoxy-4-hydroxyphenylglycol (MHPG, a major
norepinephrine metabolite) levels were quantified using high-performance
liquid chromatography (HPLC) with electrochemical detection, as described by
Höglund et al. (2000).
Samples were quantified by comparison with standard solutions of known
concentrations and corrected for recovery of the internal standard using HPLC
software (CSW, DataApex Ltd., the Czech Republic). The ratio of
[metabolite]/[parent monoamine] was used as an index of brain monoaminergic
activity. This is a more direct index of monoaminergic activity than brain
levels of monoamine metabolites per se, since variance related to
tissue sampling, and differences related to total levels of the parent
monoamine and its metabolite, are reduced
(Shannon et al., 1986
).
Owing to the presence of interfering unidentified peaks in the chromatogram we were unable to quantify MHPG in the telencephalon and hypothalamus.
Blood samples were assayed for cortisol, ACTH and -MSH levels.
Cortisol analysis was performed directly on Arctic charr plasma without
extraction, using a validated radioimmunoassay (RIA) modified from Olsen et
al. (1992
) as described by
Winberg and Lepage (1998
).
Plasma concentrations of ACTH were determined by RIA as described previously
(Balm and Pottinger, 1993
;
Balm et al., 1994
) and plasma
concentrations of
-MSH following Balm et al.
(1995
).
Statistical analyases
All data are presented as means ± S.E.M. and, since no differences
were observed between the two experimental rounds, all values were pooled. The
MannWhitney U-test was used to investigate differences in the
number of aggressive acts performed on the black and white backgrounds. Data
on plasma concentrations of -MSH, ACTH and cortisol, on brain levels of
monoamines and monoamine metabolites, and on ratios of monoamine metabolite to
parent monoamine concentrations (i.e. [5-HIAA]/[5-HT], [DOPAC]/[dopamine] and
[MHPG]/[norepinephrine]) were subjected to two-way multivariate analysis of
variance (MANOVA), with social rank or control and background colour as
dependent factors. In the case of skin colour data, a repeated-measures MANOVA
was performed. If significant effects were indicated by variance analysis, the
Sheffé test was used to investigate differences between fish of
different social rank and differences between interacting fish and
controls.
To investigate the relationships between [MHPG]/[norepinephrine] and plasma
[ACTH], linear regression analysis was performed. In addition, a stepwise
multiple regression analysis was performed to investigate correlations between
plasma [ACTH], [-MSH] and skin darkness.
To fulfil the assumption of normal distribution, data on plasma concentrations of ACTH and cortisol were log-transformed, whereas [MHPG]/[norepinephrine] ratios were subjected to arcsine transformation. All statistical analyses were performed using Statistica 5.1 (StatSoft Inc.) software.
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Results |
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Effects of social interaction and background colour on skin
darkness
The skin darkness of isolated controls and of dominant and subordinate fish
kept on a white or a black background are shown in
Fig. 2. Prior to social
interaction, there was no significant difference in skin darkness between fish
subsequently becoming dominant and subordinate (P=0.99, on white
background; P=0.96, on black background) or between fish that became
dominant (P=0.74, on white background; P=0.99 on black
background) or subordinate (P=0.38, on white background;
P=0.43, on black background) and controls. However, background colour
had a significant effect on the skin darkness of the fish
(F1,33=27.3, P=0.0009); fish kept on the black
background were darker than those kept on the white background. Social
interaction on the white background had a significant effect on skin colour
(F3,33=6.23, P=0.025) and resulted in a
significant skin darkening in subordinate fish (P=0.0015). Moreover,
following social interaction on the white background, subordinate fish were
significantly darker than dominant fish (P=0.031). Dominant fish on
the white background were brighter than dominant fish kept on the black
background (P=0.0033). There were no significant differences in skin
darkness between controls and dominant fish (P=0.99) or subordinate
and dominant fish (P=0.35) on the black background following social
interaction (Fig. 2).
|
Effects of social interaction and background colour on plasma levels
of cortisol, ACTH, -MSH
Plasma [cortisol] (F2,37=7.60, P=0.0017) and
[ACTH] (F2,37=12.90, P<0.0001) were
significantly affected by social interaction, with subordinate fish tending to
show the highest levels (Fig.
3A,C). Plasma [-MSH] was not significantly affected by
social interaction (F2,35=1.35, P=0.270)
(Fig. 3B). Moreover, there were
no significant effects of background colour on plasma [cortisol]
(F1,37=0.19, P=0.66) or [ACTH]
(F1,37=0.69, P=0.410)
(Fig. 3A,C). Plasma
[
-MSH] showed a non-significant trend (F1,35=3.20,
P=0.083) towards elevated levels in fish kept on the black background
(Fig. 3B). There was no
significant effect of social interaction and background colour combined on
either plasma [cortisol] (F2,37=2.01, P=0.15) or
[
-MSH] (F2,35=1.35, P=0.78)
(Fig. 3B,C). However, there was
a trend towards elevated plasma [ACTH] (F2,37=2.67,
P=0.082) in subordinates on the white background as compared to
subordinates on the black background (Fig.
3A), but this trend did not reach the level of statistical
significance.
|
|
Effects of social rank and background colour on brain monoaminergic
activity
There were no significant effects of background colour on [5-HIAA]/[5-HT]
ratios in any brain part (Tables
1,
2). However, background colour
had a significant effect on telencephalic [DOPAC/[dopamine] ratios
(F1,37=6.17, P=0.017), fish kept on the black
background showing higher values than fish on the white background (Tables
1,
2). In the optic tectum there
was a significant effect of background colour on [MHPG]/[norepinephrine]
ratios (F1,32=7.10, P=0.012), fish on the white
background showing a tendency towards elevated values (Tables
1,
2). However, there was no
significant effect of background colour on [MHPG]/[norepinephrine] ratios in
the brain stem (Table 2).
|
Social interaction had significant effects on brain [5-HIAA]/[5-HT] ratios (Tables 1, 2). Specifically, significant effects of social interaction were observed on [5-HIAA]/[5-HT] ratios in the brain stem (F2,33=3.46, P=0.043), hypothalamus (F2,28=4.18, P=0.026) and optic tectum (F2,32=4.9, P=0.014), subordinate fish tending to display elevated [5-HIAA]/[5-HT] ratios.
The [MHPG]/[norepinephrine] ratios in the brain stem (F2,33=7.88, P=0.0016) and optic tectum (F2,32=7.3, P=0.0025), were also significantly affected by social interaction, subordinate fish showing elevated [MHPG]/[norepinephrine] ratios (Tables 1, 2). There were no significant effects of social interaction on brain [DOPAC]/[dopamine] ratio (Tables 1, 2).
The brain stem [MHPG]/[norepinephrine] ratio was also affected by background colour and social status combined (F2,33=4.83, P=0.014), with elevated values in subordinate fish kept on the white background as compared to dominant fish (white P=0.038, black P=0.012) and controls (white P=0.0064, black P=0.038) on either the black or white background (Tables 1, 2). Moreover, in all fish taken together, brain stem [MHPG]/[norepinephrine] showed a significant correlation with plasma [ACTH] (r=0.52, P=0.0008).
Effects of social interaction and background colour, as well as the combined effects of these dependent variables, on brain ratios of [monoamine metabolite] to [parent monoamine] (i.e. [5-HIAA]/[5-HT], [DOPAC]/[dopamine] and [MHPG]/[norepinephrine]), were all reflected in similar changes in the concentration of the metabolites. Brain levels of monoamine neurotransmitters, in contrast, in most cases remained relatively constant. However, in the optic tectum, [dopamine] was significantly affected by background colour and social interaction, but not by background colour and social interaction combined (Table 2). Similarly, background colour and social interaction had significant effects on telencephalic [5-HT] and [norepinephrine], respectively (Table 2).
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Discussion |
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O'Connor et al. (1999)
showed that Atlantic salmon (Salmo salar) parr display darkening of
the body and sclera in response to social subordination when interacting in
pairs on a light-coloured substratum. In their experiment, they observed a
sudden change to a darker colour, occurring at the moment a fish stops being
aggressive and becomes subordinate. In response to this darkening of the
subordinate fish, the behaviour of its dominant opponent immediately changed
and, as a result, the number of attacks on the subordinate rapidly declined.
Thus, darkening of the body colour appears to act as a social signal
announcing defeat and/or subordinate social status in both Atlantic salmon
(O'Connor et al., 1999
) and
Arctic charr. However, the higher number of aggressive acts observed in
dominant fish on the white background in the present study could also be
related to the fact that subordinate fish are more visible against a pale
background. This explanation is less likely since the frequency of aggressive
acts displayed by the dominant fish declined over time as the subordinate
darkened and thus became even more visible against the white background.
In Arctic charr, skin darkening of subordinates appears to be related to
the chronic social stress experienced by subordinate individuals and is
possibly mediated by a stress-induced elevation in plasma levels of
-MSH (Höglund et al.,
2000
). In the present study, there was a significant correlation
between plasma levels of
-MSH and skin darkness, even though the
effects of social rank or background colour on plasma levels of
-MSH
did not reach the level of statistical significance. A visual social signal
reflecting the activation of the physiological stress response has also been
reported in the lizard Anolis carolinensis
(Summers and Greenberg, 1994
;
Korzan et al., 2000
). However,
in A. carolinensis, the signal (darkening of the eyespots) indicates
social dominance and reflects an acute elevation of plasma catecholamine
levels. In Arctic charr, darkening of the body colour seems to reflect chronic
HPI axis activation, lasting as long as the stressor, i.e. the dominant fish,
is present (Höglund et al.,
2000
). The darkening of the body coloration and sclera of
subordinate Atlantic salmon may be a less persistent but more rapidly
activated response (O'Connor et al.,
1999
). Rapid changes in body coloration, and the visual pattern of
the body, signalling intent or motivational state during agonistic
interactions, are often mediated by neural mechanisms (e.g.
Demski, 1992
) or by rapid
changes in circulating plasma catecholamine levels
(Bentley, 1998
). The technique
used to quantify skin darkness in the present study, involving netting and
immobilisation of the fish, did not allow us to study rapid stress-related
changes in body coloration or visual pattern of the body mediated by neural
mechanisms or circulating plasma catecholamines.
Social subordination is stressful and is known to affect brain
monoaminergic activity (Winberg and
Nilsson, 1993). In the present study, we observed an elevation of
brain [5-HIAA]/[5-HT] ratios in subordinate fish, which agrees well with
earlier studies (Winberg and Nilsson,
1993
). Together with an activation of the brain 5-HT system,
subordinate fish also showed an activation of the HPI axis, as indicated by
elevation of plasma levels of ACTH and cortisol. The central 5-HT system is
believed to stimulate HPI axis activity, and it has been suggested that brain
5-HT plays a key role in the control and integration of behavioural and
neuroendocrine stress responses in both teleosts
(Winberg and Nilsson, 1993
;
Winberg et al., 1997
;
Winberg and Lepage, 1998
) and
mammals (Chaouloff, 1993
;
Dinan, 1996
).
Brain [MHPG]/[norepinephrine] ratios in subordinate fish on the white
background followed the same pattern as [5-HIAA]/[5-HT] ratios, and there was
also a significant positive correlation between [MHPG]/[norepinephrine] ratios
in the optic tectum and plasma [ACTH]. In mammals, stress is known to activate
the brain norepinephrine system (reviewed by
Stanford, 1993), and
Øverli et al. (1999
)
reported elevated brain [MHPG]/[norepinephrine] ratios and a positive
correlation between brain [MHPG]/[norepinephrine] ratios and plasma cortisol
levels in subordinate rainbow trout. Furthermore, in agreement with the
results of the present study, Höglund et al.
(2000
) observed a strong
relationship between the [MHPG]/[norepinephrine] ratios in the optic tectum
and plasma [ACTH] in Arctic charr following 5 days of social interaction on a
pale background. In the present study, we observed a significant elevation of
brain stem [MHPG]/[norepinephrine] ratios in subordinate fish kept on white
background, and the observation that plasma [ACTH] and [cortisol] followed the
same general pattern as brain [MHPG]/[norepinephrine] ratios supports the
suggestion that the central norepinephrine system plays a role in the
regulation of the teleost HPI axis.
Pale background colour, resulting in an elevation of plasma concentrations
of melanin-concentrating hormone (MCH) and a decrease in plasma levels of
-MSH, has been reported to have a suppressive effect on the
stress-induced elevation of circulating plasma concentrations of cortisol and
ACTH in rainbow trout (Oncorhynchus mykiss)
(Baker and Rance, 1981
;
Gilham and Baker, 1985
;
Baker et al., 1985
). However,
in the present study, subordinate fish kept on the white background showed a
tendency to higher plasma [ACTH] and [cortisol] than subordinates on black
background. Moreover, the effect on brain stem [MHPG]/[norepinephrine] ratios
was only observed in subordinates on the white background. Thus, fish on the
white background seemed to display a more persistent stress response, which is
probably explained by the fact that subordinates on the white background were
exposed to a more intense social stress, as a result of the greater number of
aggressive acts performed by the dominant fish. Unfortunately, in the present
study, the amount of plasma available did not allow us to quantify plasma
levels of MCH.
In the present study, social subordination resulted in skin darkening, but
only in fish interacting on a white background. The lack of skin darkening in
subordinates on a black background could be due to the lower levels of
aggression and thus reduced levels of social stress experienced by
subordinates on the black background, compared with those on the white
background. Another explanation for the lack of skin darkening in subordinates
interacting on a black background could be that fish acclimated to a black
background had reached a maximum level of skin darkness and could not become
darker in response to social subordination. The control of -MSH release
from the pituitary pars intermedia is multifactorial and is not fully
understood, but there is evidence to suggest that pituitary
-MSH is
under inhibitory control by dopamine and norepinephrine, by nerves projecting
down from hypothalamus to the pars intermedia of the pituitary
(Bentley, 1998
). In the present
study, we observed a tendency to higher plasma levels of
-MSH in fish
kept on a black background, but there was no indication of any decrease in
hypothalamic dopamine or norepinephrine activity in these fish.
In conclusions, the results of the present study further support the
hypothesis that skin darkening serves as a social signal in Arctic charr,
acting to reduce unnecessary fights and energy loss in an established
dominance hierarchy (O'Connor et al.,
1999; Höglund et al.,
2000
). Fish on a white background showed a brighter skin colour
and in these pairs the dominant fish performed more aggressive acts than did
dominant fish on a black background. This observation may be explained by a
dark fish representing less of a threat, and thus eliciting less aggression,
than a pale conspecific. Higher levels of aggression resulted in a more
intense social stress, as indicated by elevated brain norepinephrine activity,
in subordinate fish kept on a white background. The more intense stress
experienced by subordinates kept on the white background may explain why
socially induced skin darkening in subordinate fish was observed only on this
background. However, another explanation could be that fish acclimated to a
black background colour had already reached a maximum level of skin
darkening.
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Acknowledgments |
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