Unit Seven: Albert F. Bennett
Animals: Form and Function

Interview: Albert F. Bennett

Albert F. Bennett is acting dean of the School of Biological Sciences at the University of California, Irvine, where he teaches courses in comparative animal physiology and activity physiology. Although much of his field and laboratory work has involved reptiles and amphibians, his general interest in metabolism and its aerobic and anaerobic support has also led him to do research on mammals, birds, and insects. His studies of metabolism have been undertaken at a variety of organizational levels, from enzymatic to organismal to ecological. Dr. Bennett's work and many of his comments in this interview support an important theme of the chapters that follow: Animals adjust to their environment over the short term through physiological or behavioral compensation and over the long term through adaptation by natural selection.

Dr. Bennett, how did you become interested in animal physiology?

Unlike many biologists, I was never one to collect grasshoppers and things like that when I was young. I liked animals and enjoyed watching nature shows on television, but it wasn't until I got into college that I began to feel biology was something I wanted to get involved with myself. As a sophomore at UC Riverside, I took a course in comparative anatomy. One particular lecture on the way lizards regulate their body temperature just struck me. I still remember walking out of that class and saying to myself, "That's one of the most interesting things I've ever heard. I really want to know more about that." I was fortunate to be able to get involved in research as an undergraduate. I worked on lizard thermoregulation, water loss in cockroaches, toad dehydration. It was exposure to all those different questions that got me excited about research and convinced me that biology would hold my interest for a very long time.

In the most general sense, your field of research is referred to as comparative physiology or as physiological ecology. Would you make a distinction between these two terms?

Yes. Comparative physiologists usually want to understand the structure and function of a given system regardless of its adaptive context. For example, the giant nerve axon in the squid is a convenient thing to study to see what you can infer from it more generally to the design of nerves in other animals. It doesn't make any difference that the axon comes from a squid. In contrast, the physiological ecologist might ask, How does that nerve function in the normal swimming of the squid? or, What are the thermal properties of that nerve in response to temperatures that a squid might encounter in deep versus surface water in the ocean? I'm interested in both of these approaches, and so are many others.

People studying general problems in physiology seem to work with some unusual organisms. Some of the motivation behind this work, although it may be unstated, is to help us better understand physiological processes in ourselves. Is it reasonable to think that we can study, say, the principles of nervous integration in a sea slug and apply them to our own nervous system?

For any particular physiological problem, there is usually a particular system that happens to be best suited to its study. You look at things in the most convenient systems possible, and then you look at the principles you developed from those systems and you try to extrapolate from them.

Sea slugs and squids are very popular for certain kinds of nervous system research. For example, in the sea slug Aplysia, we can see an oscillating neural circuit when it swims. Does this mean that a similar system might exist in mammalian spinal cords? In fact, it does. There are such oscillatory systems there. But they might be very difficult to find if you had just gone in looking for them in a mammal to begin with.

If you open yourself up to the concept that there are a lot of design similarities among animals, you can make progress more rapidly. You can perfect techniques that can be miniaturized or carried out under different circumstances in a mammalian system. If, on the other hand, you try to jump into the most complex system right away, you may not be able to figure it out.

Much of your research has concerned metabolic components of physical activity. Could you elaborate on the relative roles of aerobic and anaerobic metabolism in vertebrates?

In vertebrates, any kind of physical activity is sustainable—in the sense that it can be carried on for more than two or three minutes—only to the extent that it is completely supported by aerobic metabolism, involving the continuous burning of fuel and the consumption of oxygen. Vertebrates use anaerobic metabolism to supplement aerobic metabolism in a couple of circumstances. When you first begin an intense activity, for example, anaerobic metabolism is instantaneously available in your muscles, and all it takes is a nerve impulse to turn things on and make them go rapidly. It takes one to two minutes of intense activity to reach the levels of oxygen transport in your system needed to support the activity aerobically. So you can begin rapid activity anaerobically and then sustain it afterward aerobically.

Does this ability to change between anaerobic and aerobic metabolism have any relevance to long-distance runners who claim to get a second wind? Is aerobic metabolism kicking in there?

I don't think so. When you go through the initial anaerobic metabolism and then aerobic metabolism takes over, we're talking about a period of about a minute. I think people who talk about second winds mean something after 15 minutes or so, a renewed burst of energy. I don't know what it is, but they're certainly not cranking on any kind of new metabolic system. We do know that there are opiate-like compounds in the brain that are released during long-term physical activity that has been sustained for 20 to 30 minutes. It's complex, and with humans you're always dealing with tremendous psychological components. I think the second wind is mainly psychological.

How do you think these two different patterns of metabolic activity, anaerobic and aerobic, might have evolved in vertebrates?

As far back as we can look, the basic patterns of anaerobic and aerobic metabolism in vertebrates were there. Primitive aquatic vertebrates relied on aerobic metabolism for the most part. The cost of locomotion in water is very low; fish can travel fairly fast, supporting themselves through aerobic metabolism alone. Anaerobic metabolism was used very rarely, only for very intense periods of activity.

When the vertebrates made the transition to land, the circumstances changed fundamentally. Terrestrial locomotion is much more expensive than aquatic locomotion. Not only do you have to support your body against gravity, which you don't have to do in water, but patterns of locomotion on land involve the acceleration and deceleration of limbs. Land animals reach the limit of their aerobic transport systems at much lower speeds than aquatic animals. For instance, a 1-kilogram salmon can swim at about 4 to 5 kilometers per hour under aerobic metabolism, but a lizard of the same size and body temperature can only go about 0.5 kilometers per hour aerobically. Anything more than a leisurely walk activates anaerobic metabolism in those animals.

With the transition to land, a metabolic system that had evolved in an aquatic environment and that had been perfectly adequate for providing oxygen in that environment now reached its limit. So, animals like amphibians and reptiles tend to lie quietly and move slowly most of the time. When they need to put on a tremendous burst of speed, that locomotion is anaerobically fueled and supported.

Now, with the evolution of birds and mammals, the metabolic and aerobic systems were greatly enhanced. A benefit of having an improved aerobic system is that you don't fatigue easily. In birds and mammals, we see levels of aerobic metabolism going way up, both at rest and during activity, allowing them to perform activities that require much more stamina and endurance. So, although reptiles and amphibians are capable of short bursts of speed fully equivalent to those of mammals or birds of the same body size, most of them aren't able to sustain this activity.

How does the anaerobically biased metabolism of reptiles and amphibians influence their escape behavior?

Their survival strategy is normally to run for a hole or someplace where they can get away. But even within a specific group, such as the amphibians, you see a diversity of strategies. Consider frogs and toads. For my class in comparative physiology, when I talk about aerobic and anaerobic metabolism, I often bring in a frog and a toad and put them in containers on the front of the desk and just leave them. Then 30 or 40 minutes into the lecture, when the students begin nodding off, I open up the containers.

The frog, of course, takes this tremendous leap and invariably hits the students in the front row, and there's absolute chaos because some in the class are usually scared of the frog, while others are trying to catch it. After three or four leaps, somebody is usually able to grab it and bring it back. The toad, meanwhile, just walks out of its container and wanders around very slowly for the rest of the lecture. It doesn't put on that intense activity, but it doesn't need to; if you've ever picked up a toad, you know what its main survival strategy is.

This whole matter of metabolic activity is related to the problem of thermoregulation. My students are sometimes confused by the terminology associated with the control of body temperature, such as cold blooded and warm blooded, homeotherm and poikilotherm, and endotherm and ectotherm. Can you clarify these terms?

I think it's best to avoid the terms cold blooded and warm blooded. For one thing, many nominally cold-blooded animals have very high body temperatures. The typical desert lizard, for example, runs around with a body temperature that would cause your brain to fry. The original terminology was homeothermic and poikilothermic. Homeo- refers to the maintenance of a constant body temperature, and poikilo- means that body temperature varies. A preferred terminology is endothermic and ectothermic, which means that the source of heat is either inside (endo-) or outside (ecto-) your body, but both sets of terms are useful.

We've talked quite a bit about ectotherms, such as reptiles and amphibians. What kind of evolutionary scenario do you think led to endothermy in birds and mammals?

First of all, you have to realize that endothermy is extremely expensive. Endotherms have resting metabolic rates six to ten times above those of ectotherms of the same size and body temperature. Overall, the rate of energy expenditure in an endothermic mode of existence, compared to an ectothermic one, amounts to something like a 20- to 30-fold difference over the course of a day. This is a very major energetic commitment for an animal.

What are the advantages of physiological mechanisms that require an animal to consume 20 times as much food? They have to be dramatic. One can hypothesize advantages once an animal is fully endothermic. But the problem, as in the evolution of many adaptations, is getting from one state to the other. An animal would have to go through intermediate stages in which it had to increase its energy costs without achieving any advantage, because raising its metabolic rate a little bit doesn't make it endothermic. It has to raise it a lot. So it's hard to see metabolism rising in small increments.

One possible explanation is that the advantages of endothermy are related not only to body temperature maintenance but also to the capacity for increased physical activity. To increase its stamina, an animal must increase aerobic metabolism, which is enhanced by a consistently warm body temperature. Increased activity made possible by aerobic metabolism offers several advantages: The animal has an increased capacity to chase food, to avoid being eaten itself, and to win a mating contest that requires more staying power. The animal that wins such a contest will be the one to reproduce. That's natural selection.

Apparently, this is what occurred during the evolution of the therapsids [the mammal-like reptiles leading up to the mammals], somewhere in the evolution of birds, and maybe in certain of the dinosaurian lines. Once aerobic levels get high enough, there are clear advantages of being able to use metabolic heat to stay warm all the time.

Do you think that cardiopulmonary adaptations common to birds and mammals (four-chambered hearts, the efficient lungs, and so on) all went along with this metabolic endothermic connection?

Yes. In these terrestrial vertebrates, there's a chain of delivery for getting gases from the external environment, bringing them into the blood across the lung surfaces, moving that blood elsewhere in the body and then removing the gases from it, and so on. But this isn't the only feasible design for a respiratory system. Insects, for instance, do things quite differently. They use their circulatory system strictly to move food and hormones from one place to another, and they deliver oxygen directly to the individual cells through a series of tubules, called tracheae, that extend throughout the body. These tracheae are capable of delivering oxygen much more efficiently and at much higher levels than our pump system.

Our heart can pump only so many times per minute and expel only so much blood with each contraction cycle. The best human athletes can increase their oxygen consumption at most 20-fold. You or I would be lucky to increase it 10-fold. But insects can increase oxygen consumption 100- to 200-fold because the gases are going directly to the tissues.

There's been a fair amount of speculation on whether the dinosaurs were ectotherms or endotherms. What's your opinion?

I tend to think they were ectothermic. A number of different lines of evidence have argued for dinosaur endothermy, but every one of them has serious flaws and exceptions to it. These were phenomenally large animals. The amount of fuel that would have been needed to support their metabolic rate if they were endothermic is absolutely fantastic.

To meet the metabolic rate of a mammal the size of a brontosaurus, for example, would take the processing of at least 200 pounds of food per hour, 24 hours a day. These were animals with only peglike structures for teeth, eating things like ferns and conifers, not high-energy material. I don't think they could do it. And even if they could, for what? To sit there and be warm? You couldn't get high levels of activity out of these animals because the morphological structures themselves wouldn't permit it. MacNeil Alexander estimated that if a brontosaurus tried to run at a speed of over 2 kilometers per hour, its bones would break.

You've worked with reptiles of all sizes. Some of your recent work has involved the saltwater crocodiles of northern Australia. Can you tell us about that research?

These crocodiles are the largest living reptiles, sometimes weighing as much as 2,000 pounds. They are fearsome animals who sometimes attack prey as large as water buffalo. The croc will lie still in the water, waiting for the buffalo to come down to drink. When the buffalo comes within range, the croc will put on a tremendous burst of speed and grab a leg or a snout and then twist. It will rip off a leg or a part of the face and then drag the animal into the water and drown it.

The conservation commission in Australia was engaged in a project of capturing and moving these animals to uninhabited areas. The commission was successful in moving the smaller crocs, but many of the large ones died in the process of capture. This was of major concern from an ecological point of view because only the big animals breed; killing off one large male can really damage the capacity of the population to propagate itself.

The animals were captured and transported after having struggled as much as they could; they just fell from fatigue. We hypothesized that the largest crocs were suffering adverse effects of blood pH change during their struggle. So the commission caught a series of animals for us, and as they brought them in, we took blood samples to see the effect of the animals' struggle on their blood chemistry. We discovered that the smaller animals became exhausted in a period of about 5 to 10 minutes. But the large animals were able to fight for well over half an hour, almost exclusively on anaerobic sources of energy. So they were building up unbelievably high levels of lactic acid, pushing their blood acidity down to pH levels completely unprecedented in any literature on acidosis.

So, we made a series of recommendations to the conservation commission about how they should handle the capture of large crocs. It's been a very challenging project.

If you had a time machine, and you could go back and do experiments with organisms that are now extinct, what would you like to study?

Well, I would be happy either in the Triassic or the Jurassic. Maybe I'd look at the evolution of mammal-like reptiles, to see how mammal-like their physiology and behavior really were. And who can deny the appeal of the dinosaurs? They dominated the entire middle age of the Earth. On both land and sea, the top carnivores and herbivores in those times were reptilian vertebrates. Fascinating animals. Experimental manipulation is something else. I'd need a thermometer and a very long pole!

A number of scientists doing basic research in comparative physiology have been funded by NASA and the Department of Defense. What sorts of potential applications might lead these government agencies to invest in this research?

One example that comes to mind is the study of the hibernation phenomenon. Physiologists are trying to understand how certain groups of mammals can go into hibernation for several weeks at a time, come out for short periods of time, then go down again. While hibernating, they maintain low body temperature and low metabolism. If we're ever going to make long-range space journeys, the space travelers' metabolism will need to be slowed down. Hibernation in humans is certainly not out of the question. Other mammals do it, and there's no particular reason why we should not be able to. Our evolutionary history is such that it wasn't necessary; we're tropical animals. But that doesn't mean that our physiological systems are incapable of doing it.

Do you have any advice for undergraduate students who hope to become professional biologists?

Get to know your professors. Talk to them and try to understand the process of science. If you're going to be a professional biologist, you're really talking about finding new knowledge. Science is a tentative operation; there's so little known in comparison to what we don't know. Once you've developed that sense, you need to start working with someone so you can get a feel for the rewards and difficulties of research. I have several undergraduate students now working in my lab. Some of them really like it, and others hate it. But if you're considering biology as a career, learning that you don't like research is as valuable as learning that you do like it.

©2005 Pearson Education, Inc., publishing as Benjamin Cummings