Bright, striped
'macho' fish win stress test in lab aquarium
BY JANET BASU
Stress can get you down.
Worse: Stress can keep you down at least that's
what happens to the male African cichlid fish when a
bigger, rowdier male controls a coveted patch of
lake-bottom territory.
In a study published Aug.
15 in the Journal of Neuroscience, a research team
led by Stanford neurobiologist Russell Fernald has shown
that continuous high levels of a stress hormone,
cortisol, work to prevent most male cichlids from
developing the bright, warlike colors, the extra muscles
and the fully mature sex organs of a dominant
"territorial" male.
Stress appears to prevent
all but the dominant males from achieving reproductive
success. Fernald said that since many species have
evolved dominant and non-dominant males, the role of
stress hormones in social systems may be widespread.
"The interesting new
thing we have found is that stress depends not only on
the social state of the individual male but also on the
stability of the community," Fernald said.
Fernald is the Benjamin
Scott Crocker Professor of Human Biology and director of
the Human Biology program at Stanford. He is also a
professor of psychology and a member of the Neurosciences
program faculty. He and members of his laboratory already
have shown that for cichlid fish, social position
determines physiology. It's not so much that the biggest,
brightest fish becomes dominant. Instead, a fish must
earn his bright "macho" colors by proving to
himself and others that he can control and defend a patch
of food-laden gravel.
Those males that prove
themselves Fernald and his students call them
"territorial" experience a dramatic
transformation, switching color within minutes from a
camouflaged sandy gray to bright blue or yellow. Within
days, they put on weight, mature sexually and sport a
threatening, warpaint-like stripe next to their eyes.
As in the movies, the
macho fish also gets the girl: He offers grazing rights
to entice breeding females to lay their eggs in a
sheltered nook within his territory. Only territorial
males have the fully developed gonads capable of
producing sperm to fertilize those eggs.
All in the head
All of this is reflected
in a patch of cells in the fish's brain that increase
eight-fold in volume while they pump out big doses of
gonadotropin releasing hormone (GnRH), the coordinator of
sexual development for all vertebrates, including humans.
Most remarkably, if a territorial fish is defeated by
another territorial male and loses his status, he loses
the symbols of status as well. The colors and eyepatch
fade, the GnRH cells in the brain shrink and so do the
gonads.
"In our lab, we have
shown that behavior influences the brain," said
Fernald. "We've seen that behavioral encounters can
modify the GnRH producing cells, and we know that this
hormone in turn triggers changes in body structures that
influence reproductive success. Now we want to know how
social behavior can produce such changes in brain
cells."
He and his students looked
at cortisol as a possible mechanism. Cortisol is the
"fight or flight" hormone, squirted out by the
adrenal gland to give an animal a sudden burst of
strength or speed so it can fight off an attacker or zip
away from a predator. Other scientists have shown that
cortisol levels remain high in the body if an animal
or a human is constantly under stress. The hormone
appears to be a trigger for many of the physiological
effects linked to long-term stress, from sour stomach to
heart disease.
Territorial rights
The Fernald lab is stacked
with aquariums equipped to imitate the conditions of life
in shallow pools of Lake Tanganyika, where this breed of
cichlid fish originated. On the aquarium floor, a layer
of gravel is piped with plastic tubing to deliver fish
food from below in the wild, cichlids sift through
gravel to eat the decaying plant matter collected there.
Overturned flower pots imitate the rocky nooks that male
cichlids defend as spawning sites in their territories.
By setting up various versions of this environment and
introducing various combinations of male and female fish,
Fernald has been able to study social behavior and the
physiological and neurological changes that it entails.
The cortisol research was
primarily conducted by three students. Helen E. Fox, a
1994 graduate of Swarthmore, worked in the Fernald lab
for two years before starting graduate studies at the
University of California-Berkeley. Stephanie A. White
earned her Ph.D. in neurosciences at Stanford this year
and is now a postdoctoral fellow at Duke University. Mimi
H.F. Kao won a Firestone Medal for her cortisol research
while earning her bachelor's degree in human biology at
Stanford in 1995. Now she is working toward a graduate
degree in neurosciences at the University of
California-San Francisco.
They tested the hormonal
response to stress by capturing the fish and taking blood
samples before returning them to the tank. First, they
determined that if a sample was taken within four minutes
after capture, cortisol levels represented the baseline
amount of hormone that was in the fish's bloodstream in
the tank, not the big spurt pumped out by the adrenal
gland during capture.
Fernald said that the
team's major finding came from an experiment where 20
male and female fish were introduced to a large aquarium,
with gravel and potsherds placed over half the floor and
the other half left bare as a refuge from territorial
wars. The fish were all new to one another; none had been
raised in the same tanks. Most of the males were still
sexually immature.
The males immediately
began vying for patches of territory. For the first few
weeks, ownership changed frequently and so did the
males' bright colors, switching on or off depending on
which male perceived himself to be the victor. Perhaps
most important, Fernald said, was the fact that no
females elected to lay eggs during this period of social
instability.
Eventually, several males
established permanent territories and began their
transformation into large, bright, dominant animals. The
other males remained almost indistinguishable from
females. That nondescript coloring has its advantages: A
non-territorial male can sneak into a dominant male's
territory by impersonating a female, and snatch extra
food.
This behavior is the same
as in Africa, where Fernald has done field work. And in
the wild, a brightly colored fish is more likely to be
snatched up by a wading bird. But Fernald's team knew
from previous experiments that if males were raised
alone, they would take on the flashy traits of a dominant
fish. What happens in social situations to suppress some
males' maturation?
The scientists found two
kinds of evidence that cortisol is at least one of the
factors mediating between behavior and physiology. Early
in the period of social instability, both territorial and
non-territorial males showed similar cortisol levels,
with males that were territorial at the time of a blood
test showing somewhat higher levels than non-territorial
males. That is consistent with cortisol's known role as a
fight-or-flight hormone, marshaling the resources needed
for a battle.
Once the social system was
stable, however, the territorial males' cortisol levels
dropped dramatically even though such fish are
constantly active, chasing away other males and enticing
females. Meanwhile, the stress hormones in the blood of
non-dominant males skyrocketed once their competitors had
control over all the available territory. Those cortisol
levels stayed high for the remainder of the study.
The differences in
cortisol levels between territorial and non-territorial
males and between stable and non-stable social situations
provide evidence that this stress hormone response tracks
both the individual's social status and the dynamics of
its social scene, the scientists concluded.
The hormone differences
also offer tantalizing evidence that cortisol might be
the mediator between the social situation and the
non-territorial males' failure to mature. Continuous high
levels of stress hormones might affect the size of GnRH
producing brain cells, Fernald said but this study
does not offer positive proof of that hypothesis. More
research, involving implants of cortisol and a cortisol
antagonist in selected fish, may answer that question in
the future.
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