LIFE at the top can be pretty stressful. If you were the Queen waiting for
the next adultery scandal in the British Royal Family, or Bill Clinton slogging
it out with Saddam Hussein on the centre stage of world politics, you’d probably
get more than your fair share of sleepless nights, and a double dose of stress
hormones to boot.
Yet when it comes to other animals that live in social groups, there’s been a
long-held assumption that those low on the pecking order are far more strung out
than those at the top. After all, the reasoning goes, subordinates must battle
for food, sex and survival. And it is the underdogs who are most likely to be
the hapless victims of aggression. Dominant animals, on the other hand, were
supposed to live a charmed life, replete with easy access to food and sex, a
loyal following of fawning subordinates, and the prospect of going forth and
multiplying far more successfully than their underlings.
The truth, it transpires, is infinitely more complex. Studies of the
behaviour of social animals living in their natural habitats, are now showing
that striving to keep the upper hand (or paw or wing) can send stress hormones
soaring, and may even limit an animal’s reproductive success. Whether it is more
stressful to be a high-ranking animal or lower down the greasy pole, it turns
out, varies from species to species, and depends on a multitude of other
factors, including whether the social group is stable or in turmoil, and even
the animals’ personalities.
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Down and out
The fallacy that life at the bottom of the heap is inevitably more stressful
grew out of studies on captive baboons, monkeys and rats during the 1950s and
1960s. The subordinate animals had chronically high blood levels of the
stress-response hormones cortisol and corticosterone. These hormones help raise
blood glucose levels for flight or fight. But if they remain high for long
periods, they suppress the immune system, kill nerve cells and trigger other
pathological changes. Other studies of both captive and wild monkeys, showed
that females at the bottom of the pecking order had fewer offspring than those
at the top. In the most extreme cases—the marmoset monkey, for
instance—the underlings were barren. The most obvious explanation was that
the subordinate animals suffered stress-induced infertility. So was born the
dogma of the stressed-out subordinate.
But earlier this year, Scott and Nancy Creel, behavioural ecologists from
Rockefeller University in New York City, reported some new observations that
flatly contradicted the received wisdom about stress and social status. The
Creels first identified each member of the hierarchy in packs of dwarf mongooses
(animals about half the size of a grey squirrel) living in the Serengeti
National Park in Tanzania, and in packs of African wild dogs (a distinct
species, not domestic dogs gone wild) living in the Selous Game Reserve, also in
Tanzania. In both species, says Scott Creel, when it comes to a fight the
subordinate animal runs away, shows its underbelly in a submissive gesture or,
“if the dominant animal pins it down, it may even pee itself”.
As well as being helpful for identifying subordinate individuals, the
animals’ urination habits proved useful in another way. Nancy Creel noticed one
dwarf mongoose urinating on a discarded rubber sandal. Banking on the mongoose
habit of urinating where another has gone before, the Creels placed the rubber
sandal—now dry, but still carrying the irresistible scent of
urine—outside the burrows of ten different mongoose packs. As they hoped,
the dwarf mongooses urinated on the sandal first thing in the morning when they
emerged. All the researchers had to do was collect the urine from the sandal
with a syringe and measure its cortisol content. They measured corticosterone
levels in the faeces of the African wild dogs.
Against all their expectations, when the Creels analysed the urine samples
they found that cortisol levels were about twice as high in dominant females
(but not males) compared with subordinate dwarf mongooses of both sexes. In
African wild dogs, corticosterone was 50 per cent higher in dominant males and
twice as high in dominant females, compared with their subordinates.
These findings led the Creels to speculate that the dominant members of wild
packs of dwarf mongooses and African wild dogs are victims of their own social
success. Because they have to keep reasserting their social status in aggressive
encounters—a vital activity because, in both species, only the dominant
animals get to reproduce—they suffer greater stress than their
subordinates.
Cage confusion
And it’s not just mammals that suffer success-related stress. Dominant
red-winged blackbirds—the ones who guard the largest
territories—have higher levels of corticosterone and testosterone than
low-ranking males without territories, according to a study by John Wingfield,
an endocrinologist at the University of Washington in Seattle.
The misconception that subordinate animals were invariably more stressed came
from observing the distinctly unnatural behaviour of animals in cages. Now,
researchers like the Creels, argue that in captivity, the meek subordinates may
suffer far more stress than they would in the wild because they never escape the
hostile advances of their superiors. In the wild, the subordinate animals can
just shuffle out of the way.
However, there is at least one striking exception to the idea that superior
animals in the wild suffer more stress. In 1982, neurobiologist Robert Sapolsky,
who now works at Stanford University in Palo Alto, California, discovered that,
much like their captive compatriots, subordinate male olive baboons living wild
in the Masai Mara National Reserve in Kenya have cortisol levels that are 66 per
cent higher than their superiors.
The explanation for the stark differences in the stress levels of subordinate
animals of different species may lie in their social lives, says Sapolsky. Dwarf
mongooses ascend the social hierarchy by biding their time, eventually
inheriting a position when another animal dies. Subordinate male baboons, on the
other hand, have to challenge a superior to a fight, and win, in order to ascend
the social ladder (female baboons are more like the mongooses—they inherit
their rank). Among male baboons, “there’s no such thing as inheriting the family
business”, Sapolsky says. “Being a subordinate wild mongoose is a much better
life than being a subordinate baboon.” So it is hardly surprising that underling
baboons suffer more stress.
Hell breaks loose
It is even conceivable that the Creels’ packs of African wild dogs and dwarf
mongooses were undergoing some dramatic, unrecognised change that put undue
stress on the dominant animals and skewed the results. That has happened before.
Early studies on captive rhesus monkeys misled researchers, who assumed that
they were monitoring a stable hierarchy. In fact they were studying societies in
turmoil, as strange animals were put in a cage together and fought tooth and
claw for positions in the hierarchy. It turns out that, although rhesus monkey
underlings suffer more stress when a society is stable, the stress of rank is
greater in periods of social disturbances.
“All hell breaks loose. Ranks shift. Social support and the psychological
advantage of being dominant go out the window,” says Sapolsky. Being a dominant
animal at such crucial times is like being “the Tsar of Russia in the spring of
1917”. The same cortisol response to stress happens when wild baboons are
captured and immobilised, and the dominant animals show a much larger increase
in their cortisol levels than the subordinate animals.
But Scott Creel argues that neither the way African wild dogs move up the
social hierarchy nor social disturbance in the packs he studied can explain away
the surprisingly stressful lives of the dominant African wild dogs. Unlike the
mongooses, both male and female African wild dogs may fight to ascend the ranks,
he says, and yet they appear to be less stressed than the top dogs. What is
more, the Creels studied the dogs for more than two years. During that time,
some of the packs were stable, and others experienced social unrest as dogs died
and others fought their way to higher ranks. In all cases, the link between high
rank and high corticosterone levels was constant.
And there is at least one more ingredient to be added to the elaborate recipe
for chronic stress in social animals: personality. Sapolsky has found that male
baboons who show a variety of socially savvy traits (for instance, they easily
distinguish non-threatening behaviour, such as a rival baboon napping nearby,
from threatening behaviour, the same rival picking a fight) have lower cortisol
levels than socially inept baboons of the same rank.
New research is also challenging a second cherished belief, that subordinates
in groups of social animals produce fewer offspring than the big cheeses.
Reproductive disturbances related to stress and stress hormones have been
recognised for a long time in humans. The best-known example, apocryphal or
otherwise, is the surge in numbers of female students seeking pregnancy tests
during their final exams. The theory goes that the stress stimulates the release
of cortisol and other glucocorticoids, which dampen down the sex hormones, block
ovulation and delay menstruation.
When it comes to long-term infertility in humans, it’s difficult to separate
the stress of not being able to conceive from the stress that may block
fertility in the first place. A 1993 study, by reproductive biologist Samuel
Wasser from the University of Washington in Seattle, got around that problem by
comparing the stress ratings of three groups of women. Those in the first group
were infertile due to hormonal imbalances (for example, they produced too little
progesterone, a hormone that is essential for pregnancy); the second had the
same hormonal imbalances but were not trying to get pregnant; and the third were
infertile as a result of anatomical problems such as scarring of the oviduct.
The findings showed that women who had the hormonal imbalances, whether or not
they were trying to conceive, scored far higher on a battery of stress
questionnaires than the women without the hormonal abnormalities. This suggests
that stress is responsible for infertility, rather than the other way
around.
Stress may also block reproduction in other primates. Last year, behavioural
ecologist Craig Packer of the University of Minnesota in Twin Cities, and Jane
Goodall, Apollinaire Sindimwo and Antony Collins of the Gombe Stream Research
Centre in Kigoma, Tanzania, published in Nature the results of one of
the largest surveys of reproduction in wild primates ever conducted. The
histories of 138 olive baboons living in the Gombe National Park (alongside
Goodall’s famous chimps) between 1967 and 1992 showed that although dominant
female baboons generally seem in better shape, and have priority when it comes
to food, the number of young they produce over a lifetime is exactly the same as
lower-caste baboons.
High-ranking female baboons suffered more late-stage miscarriages, and a
proportion had severe fertility problems. One huge, aggressive, top-ranking
female baboon called Lotus had only one pregnancy—which she then
miscarried—over her whole 20-year life, says Packer. Overall, such factors
cancelled out the greater fecundity of the fertile high-ranking females, who
tend to give birth more frequently, and are more likely to have infants that
survive compared with low-ranking females.
Outrageous anomalies
But the link between the stress of success and infertility is contentious.
Primatologist Jeanne Altmann of the University of Chicago, together with
Sapolsky and Paul Licht of the University of California in Berkeley, have found
no difference in the rates of miscarriage between the dominant and subordinate
members of a troop of yellow baboons living in Amboseli National Park in Kenya.
And dominant wild African dogs and dwarf mongooses, despite their stress levels,
reproduce far more effectively than their subordinates. “It’s a mystery,” says
Scott Creel. “Everything we know about stress hormones tells us [that the
mongooses and dogs] should reproduce poorly, but they do just fine.”
And even if dominance is linked to a reduced ability to reproduce in some
species, that doesn’t necessarily mean that giving up your old domineering ways,
and the stresses associated with them, will ensure that you’re a reproductive
whiz. Packer takes the controversial stance that reproductive success is reduced
by the hormones that enable animals to be aggressive and dominant in the first
place, not by the stress created by that dominance.
Take female spotted hyenas. From the moment they are born, these animals are
notoriously aggressive, (see New Scientist, 5 March 1994, “When hyenas
kill their own.”) probably due to the extremely high levels of testosterone
produced by the placenta, and by the female hyena pup’s own high levels of
“male” hormones. These hormones also masculinise the clitoris so that it is
almost indistinguishable from a hyena penis. In Packer’s words, the female hyena
is “outrageous, obnoxious…and anomalous”.
The rarity of such extreme aggression in female animals suggests that the
trait has a downside severe enough to stop it arising in most species, says
Packer. So although the female hyena’s macho attitude and appearance has
distinct benefits for an animal that hunts in large packs and has to fight for
its share of the carcass, it exacts a cost. Females have to give birth through
the penile structure. To add insult to injury, the birth canal is tortuously
long and even doubles back on itself. That makes giving birth both painful and
dangerous. First-time mothers have a 9 to 18 per cent chance of dying during
labour, according to studies on captive and wild hyenas by behavioural
ecologists Laurence Frank, Mary Weldele and Stephen Glickman from the University
of California in Berkeley.
“It’s a knife-edge,” says Packer, who argues that high levels of androgens
may also be the root cause of the reproductive dysfunction seen in some
high-ranking female baboons. “There is some advantage to dominance. But
there is a high cost, too.” At any rate, life at the top may not be all it’s
cracked up to be.