by Denyse O'Leary
We've all heard about fight or flight. Every popular science pundit can explain it. It makes great film footage. But are those really the animal's only options?
How zoologist Norbert Smith, now retired, got into chasing alligators for research is a story in itself: He was out collecting frogs and snakes with his graduate Ecology class at Baylor. From a boyhood spent with animals, he spotted the distinctive eye-shine of an alligator. He offered to catch the class an alligator - an offer they dismissed because they had not seen the gator themselves. Besides, he was the newest student and from Oklahoma. He must have been mistaken ...
But, he recounts, "Undaunted, I called the alligator by imitating the grunting alarm call of young alligators and splashed my hand in the water. The alligator immediately swam midway across the pond toward me. It then swam right up to my feet and I jumped on it."
He used the opportunity to demonstrate interesting adaptations of alligators for the class, but - much more - he could actually bring them in. That got his profs' attention.
Following the gators wherever they go
One problem with studying animals is that no one knows what they do when no human is around. However, modern technology comes partially to the rescue in the form of telemetry (tracking a remote animal that has been fitted with a radio device).
Having done well in electronics in the Air Force, Smith was interested in using telemetry on submerged alligators. He developed greatly improved telemetry equipment for monitoring rattlesnakes. He then acquired a large alligator at the Welder Refuge, fitted it with a collar, and released it into Big Lake.
He was attempting to test the way in which alligators regulate their body heat (thermoregulation) for his MS thesis. To do this he would follow the alligator for days, observing it from a blind or, when necessary, from a boat.
A great deal was riding on the experiment because, contrary to the widely accepted "reptilian brain" theory of intelligence, the alligator is intelligent. Once escaped, it is gone ... hard to recapture.
At first, things went well. The telemetered alligator behaved like two other large alligators Smith was able to observe, which meant that fitting the transmitter had not altered its behavior, thus the data would not be distorted. Indeed, the data coming back about the gator's temperature and heart rate looked normal.
The fight or flight response has been studied for over 70 years, and Smith simply assumed that alligators would follow this pattern. But something unusual happened.
According to the textbooks, the gator's metabolism is supposed to slow down when it submerges in water (diving brachycardia). That certainly made sense, in principle. Alligators can hold their breath for up to two hours without drowning; diving might well be the trigger to start conserving energy.
But no one had actually studied the free ranging diving alligator before. And this gator's heart rate did not slow down.
At first, Smith was astounded. "It violated everything I had been taught as a budding physiologist. ... My telemetered alligator had obviously NOT read the books. It was free-ranging in its natural habitat. Its behavior matched that of non-telemetered alligators I knew it was healthy and the telemetry system was working. Everything checked out. It was just not conforming to the rules."
Not only that, the gator began to travel. That meant Smith had to follow it, living far from the comforts of civilization on a flat-bottomed boat. It was worthwhile, because hundreds of measurements confirmed the original one.
Smith was forced to conclude that the textbooks were wrong. The alligator does not slow its heart when it dives.
On the other hand, was it just an unusual gator? That was hard to tell; it had slipped out of range.
Maybe. At Lake Pollito, Smith spotted the gator again, returning to the water with a freshly caught raccoon in its mouth. It had to be the same gator; the telemetry collar was still secured around its neck.
But this time, something even more unusual happened. Accidentally frightened by another wildlife biologist working in the area, the submerged alligator suddenly lowered its heart rate from 32 beats per minute to merely 2. About half an hour later, the gator's heart rate had returned, in slow stages, to normal.
Smith writes, "It was obvious that Will [the other biologist] frightened the alligator. His canoe passed within a few yards of the alligator, yet its heart slowed instead of speeding up. Everyone knows that heart rates speed up when frightened. What is going on?"
Suddenly, the situation became clear, and needed only confirmation: The alligator's heart rate slows - not as a result of submergence, as was believed from laboratory studies - but as a response to fear.
In fact, when alligators were forced under water in the lab studies, it was passive fear rather than diving that slowed their hearts.
Laboratory data are also complicated by the fact that caged alligators begin the interaction by responding aggressively toward approaching humans, thus increasing their heart rate. To clearly exhibit the slowed-heart "passive fear" response, as Smith calls it, the alligator must be both submerged - in a safe hiding place - and frightened at the same time. Two hundred "evoked fear" episodes later, working with four different alligators, confirmed this.
Mammals too may show passive fear response
Smith discovered from library research that a number of other animals slowed their hearts in response to threats. "Field mice slow their heart rate and even lower their body temperature when a shadow passes overhead. Ground squirrels slow their hearts while hiding. Newborn deer fawns drop to the ground, freeze, and slow their hearts when approached by man or dog."
There was plenty of supporting data in the literature, he discovered, but it was all scattered. No one was putting the data together to challenge the "fight or flight "paradigm, dominant for 70 years. Researchers assumed that any response at all involved an increase in the metabolic rate, even though a reduced metabolism might actually be highly adaptive.
Smith's additional work led him to make many discoveries in the complex systems by which alligators regulate their body temperature, and led to many publications in journals. But he was most interested in his accidental discovery of passive fear. He and a number of colleagues went on to study it in a variety of animals.
One question was, what benefit did slowing the metabolism confer on a mammal? The benefit to an alligator is obvious: It limits the need for oxygen and thus increases the amount of time the gator can spend in a safe place under water. Smith's research with burrowing mammals suggested another possibility as well: Woodchucks only showed the slowed heart rate after they had retreated to their burrows. Threatened burrowers are known to plug their holes, thus decreasing the amount of oxygen in the burrow, often dramatically. A slower metabolism might keep them alive much longer. Further studies in wild rabbits, both in the wild and in the lab (using atropine and propranolol), confirmed the passive fear response. Smith went on to study it in swamp rabbits, squirrels, chipmunks, turtles, opossums, ground sloths, and a South American marsupial, the timbu.
He learned a variety of interesting things. Swamp rabbits for example, who are adapted to water, do not slow their hearts during a voluntary dive - just as that original alligator had not. So the rabbits had not read the textbooks either.
Why lab studies may mislead investigators
Smith learned to be highly skeptical of the use of lab animals in behavior studies on fear (p. 41). The insurmountable problem that, after generations of breeding for docility, such animals can no longer reliably be frightened. Indeed, tame lab rabbits generally did not exhibit the crouch-and-hide behavior associated with the slowed heart rate in wild rabbits.
Actually, the behavior would probably never have been discovered except for telemetry done on wild animals. "There is no doubt in my mind that this discovery would have eluded me had I trained in the more traditional laboratory environment" he argues. However, the increasing use of wild animals in laboratory studies, to try to overcome this problem, does not necessarily resolve it. For example, fox squirrels in the lab failed to show the passive fear response that they showed in the wild, perhaps because the lab does not offer them the "safe hiding place" mode that triggers the reaction. As Smith puts it, "Wild animals may certainly be kept alive and healthy under laboratory conditions, but their behavioral and physiological responses to threat are clearly altered by confinement."
What about "playing dead"?
Some have dismissed as unsubstantiated "American folklore" the idea that the Virginia opossum "plays dead" when threatened. Smith and Norwegian colleague Geir Gabrielsen wanted to investigate. If clearly documented, the "dead" feint might be best explained as a variation on the passive fear response.
At first, the researchers just could not get the opossums to cooperate, no matter how they tried to frighten them. The opossums would respond aggressively for about a minute and then, when released, they just ran away.
But then the researchers got lucky. Smith's dog was with him, and she suddenly mouthed an opossum. It immediately lapsed into the classic state called "playing possum," that includes hypoxia (mouth parts turn blue from lack of oxygen). So, annoyance by humans did not trigger a passive fear response in the opossum, but seizure at the neck for the "killing bite" by a natural predator triggered it immediately.
"Cruelty to animals" charge
But the two colleagues' accidental discovery was largely submerged by the politics of research. Even after 100 technical publications, they could not get their research published in the prestigious American Journal of Physiology because - even though no opossum had been hurt - the editor feared pressure from animal rights activists on account of the fact that a dog attack had triggered the opposum's lapse into deep unconsciousness. The paper was eventually accepted by an obscure Norwegian journal. Smith comments that an unfortunate outcome of this avoid-controversy-at-all-costs attitude is that, as his colleague Geir has noted, understanding the triggers for these states might help shed light on medical problems such as Sudden Infant Death Syndrome.
Actually, overall, it's too bad that humans can't do the passive fear response, at least not as a useful adaptation. Drowning swimmers or trapped miners could certainly benefit from it.
However, understanding the response might still be useful for medicine, as Smith notes, for its possible role in understanding such states as hypertension, that involve changes in metabolic functions. (This very common disorder, involving chronic high blood pressure, is called "essential hypertension" because its origin is not known.)
Smith ends his book with many questions and a plea. For example, a question: Two-week-old white tailed fauns display the heart-slowing passive fear response - but they lose it a week later, in favor of heart-accelerating flight. How? His plea is for multi-disciplinary research, because his own thirty years of experience clearly demonstrates the limitations of the present research environment.
Buy E. Norbert Smith, Passive Fear: Alternative to Fight or Flight (New York: iUnverse, 2006), and it's only $13.95.
Toronto-based Canadian journalist Denyse O'Leary (www.designorchance.com) is the author of the multiple award-winning By Design or by Chance? (Augsburg Fortress 2004), an overview of the intelligent design controversy. She was named CBA Canada's Recommended Author of the Year in 2005 and is co-author, with Montreal neuroscientist Mario Beauregard, of the forthcoming The Spiritual Brain (Harper 2007).
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