Interview: Karel Liem

It is a common story among scientists: Some unexpected, unexplained observation captures a curious mind and focuses its general interest in nature onto a particular field of science. In the case of Karel Liem's research career, the defining moment was a nighttime encounter with a peculiar animal. Dr. Liem is now the Henry Bryant Bigelow professor of ichthyology (the study of fishes) at Harvard University. He is recognized for both his creative research as a vertebrate biologist and his inspiring lectures as a general biology teacher. Professor Liem is past president of the American Society of Zoologists and a recipient of the Phi Beta Kappa Teaching Award, Harvard's highest commendation for classroom excellence. His unique talents as scientist and teacher are evident in this interview.

Most young people like animals, but only a small fraction of students choose zoology as a career. What experiences focused your studies on fishes and other animals?

I was fascinated with animals very early on because I grew up in Indonesia, which is a beautiful example of biodiversity in the tropics. I would look at the geckos crawling around on the ceiling, upside down, and try to figure out why they didn't fall off. Or flying lizards. I was always fascinated by the incredible adaptations that the animals had, even though I didn't know anything about adaptations. I also was interested in the behavior of animals.

I got into fish when I went to college. In my senior year I went on a trip to collect frogs for eating purposes; the class was going to have frog legs for dinner. We went out at night with lights in the rice fields around Bandung on the island of Java to collect frogs. As I walked past a grassy field I encountered a migration of animals across the field. I didn't know what they were; they looked like snakes, but they were not snakes. I picked up a dozen of these creatures and put them in a bag. We collected the frogs and had a wonderful frog-leg dinner. The next day I took the bag to the lab and emptied these organisms "X" into the sink. They were alive and well. I just could not figure out what they were. They were eel-like, about 2 feet long. My advisor, who came from the United States, had never seen any animals like these. He looked at them carefully and asked, "What are these?" I said, "I have no idea what they are." And he said, "Well, you find out."

I found out they were fish, air-breathing fish, which were migrating over land. I wondered, what made them get out of the water to find another pond? How do they survive on land? How do they find their way? Surely a fish in tall grass can't see ahead. They have very tiny eyes. I was really interested in those questions, so I decided to do a thesis on the air-breathing fishes for my master's degree. That's the way I got into ichthyology. It was completely accidental. Originally I was going to study plant diseases. But that little accident changed my entire goal in life. Instead of being a plant pathologist, I became an ichthyologist.

Do air-breathing fishes, such as the species you studied in Indonesia, provide any clues about the vertebrates' evolutionary trek onto land?

Originally people thought, on the basis of geological evidence, that the origin of terrestrial vertebrates was triggered by drought conditions. According to this idea, bodies of water were drying out and the fish started to crawl out from the disappearing ponds and make their way to a better pond. I've done a considerable amount of research on what triggers a fish to get out of the water, and I think it's definitely associated with the drying out of ponds. But there's more to it. During the dry season, the fish would stay in water as long as possible! When the water disappeared, they burrowed into the mud. For example, lungfishes will estivate.

What triggers air-breathing fishes to wander on land is competition. I have done a series of experiments in which I varied the population densities in ponds. When the population is too dense, competition for food or nest sites becomes very intense, triggering the fish to abandon the pond, but only when conditions are wet on land.

The important thing is that these fishes migrate over land only when it's very wet outside: after a rain, for instance, when the grass is wet. I think I have supported the hypothesis that vertebrates made the transition to land during hot, very wet, and humid tropical conditions. Desiccation was probably the greatest problem facing organisms that were originally aquatic as they invaded terrestrial habitats. Air breathing is not a problem. Fishes can adapt easily, because most air-breathing fishes are bimodal; they engage in both gill and lung breathing. If the oxygen concentration is too low in the water, they just take up an air bubble and breathe air. So that's not the problem. I think the major problem of getting on land is desiccation.

As far as locomotion goes, I think the fishes were very well adapted to develop locomotory limbs, so to speak, because they already had very fleshy, lobed fins with bony elements in them. Even now, there are recent fishes that can walk with their fins. There is also a problem with water conservation. When fishes get on land, instead of the kidneys pumping water out all the time when they are in fresh water, they reverse that function and retain water, just like our kidneys are doing.

What about the energy it takes to move around on land? Is it harder work to travel on land than it is in water?

Very much so. Gravity and locomotion on land have probably been major constraints on amphibians, especially as they also depend so much on the external temperature to keep their metabolism up. But there are tremendous food resources on land. Vertebrates basically invaded a completely empty niche and got tremendous food resources in all the available terrestrial invertebrates. I imagine that the move onto land was kind of a compromise.

Does the descent of terrestrial vertebrates from fishes teach us any general lessons about how evolution works?

Yes. I would say it shows how existing structures may have very different functions later in evolution. Major evolutionary innovations often originate from preexisting structures.

You have also studied sex reversal in certain species of fishes. How do you explain this phenomenon?

It has something to do with fitness. There's a lot of debate about what we mean by "fitness" in evolution, but everyone agrees that it depends on how many surviving offspring you produce. I always tell my athletic students that in Darwinian terms they are less fit than I am because I have children and they don't. At the heart of sex reversal is fitness. So reproductive biology is definitely well suited for "why" questions. There must be an explanation for sex reversal in terms of how it has increased the fitness in fishes that start life as a female and end life as a male and vice versa.

I worked on the same mud eel that was going from one pond to another. This species, Monopterus albus, turned out to be a gold mine, because it was also a sex-reversing fish. It starts as a female. Every one of these eels is born as a female; not a single individual is born as a male. Then, after being functional females for several years, they start changing sex. By the age of 4 to 6 years, every individual has become a male.

I came up with a hypothetical explanation for this. Since this fish often inhabits ponds that dry out, when the rainy season arrives they must immediately start reproducing. That's the best time in terms of food resources, water availability, and nest sites. So it is advantageous for them to reproduce right away. Now, I hypothesize that if you are born as a female first, the population is very much skewed in favor of females: there are many more females than there are males. What happens to such a population when a large pond becomes subdivided into small patches during the next dry season? Individuals trapped in very small ponds with insufficient food resources would change sex from female to male. So functional males are produced. Other populations in better ponds remain all female. When these ponds overflow and fuse together at the next rainy season, the populations of females and males are ready to reproduce, just when the environment is best. I tested this hypothesis in the laboratory. When populations are starved, sex reversal begins at an even earlier age. It is evidence that adverse conditions do trigger sex reversal.

In other species of fishes that switch sex, the causes may be entirely different. For example, some small sea basses live in schools with only one male and about 24 females. Such a reproductive school remains stable. But if you take the male out, one of the females will become a male almost overnight. Really amazing! It's always an alpha female, a boss that becomes the male. Apparently it is the macho behavior of the male that keeps females female. As soon as the female no longer receives the macho behavior of the male, she becomes macho herself and becomes a male.

So how do we come up with a unified theory for all this? Biologists like to be like physicists: they would like to formulate a general theory that explains all cases of sex reversal in fishes. But in biology, there are a lot of particularistic explanations, explanations that apply only to a specific case. I would suggest that this is true for the phenomenon of sex reversal. There might be many different explanations. That frustrates biologists, but I think it makes biology fascinating.

You mentioned schools of sea bass. How does schooling benefit fishes?

Many fishes do school, and the general consensus is that it is basically a defense against predators. It has a confusing effect on the predator. When the predator starts zeroing in on a particular fish that somehow manages to disappear in a school, the predator has a hard time continuing that strike and misses. And schools also function as extended eyes: the individuals on the periphery see something that individuals in the center are not aware of, and the whole school moves as an ensemble. It's like little pseudopodia sticking out of the school, and these may actually determine the movement of the school. There might not be an individual leader, but there might be a leading "pseudopod" which determines whether to retreat or whether to expand and to move. That's the current theory about schooling.

Dr. Liem, much of your research is associated with an approach known as functional morphology. What is a functional morphologist?

Functional morphology really meets adaptation head on, I believe, at a level that other fields do not. Functional morphologists try to figure out how a system works, how efficiently it works, and how its performance relates to its natural habitat and in competitive interactions. We're using, basically, engineering principles and physiological principles to explain animal structure. Functional morphologists also consider the evolutionary aspects of structures.

Ultimately, functional morphologists are interested in the interactions between structures within components of an organism, for example, the leg or the head. It's the interactions between parts that may constrain the functional expression of the component. Emphasizing the nature of interactions between structures serves as a model of how to approach organismal biology. This principle also applies to ecology, where we have different interacting factors. It is basically a network of constraints, and we would like to know how a change in the nature of the interaction may release a constraint, which results in a greater diversity. It can also be applied to the biosphere. That's an integrated system of a multitude of factors.

I think functional morphology can lead the way in research strategies. Instead of searching for the optimal solution, we are searching for the nature of how components are interconnected and how these interconnections limit the functional performance. The interconnections may be of a mechanical nature. But more importantly, the interconnections may be related with developmental patterns that are genetically programmed.

Have the ideas and methods of functional morphology changed much in the past few decades?

Yes, tremendously so, I believe. There are two fronts that have revitalized morphology. One area is technology. We now have incredible tools to determine function. But it's not only technology, of course. We have also made progress conceptually. We are now dealing with the notion of adaptation in a quantitative way, in a measurable way. The combination of the technology and this conceptual progress, I think, has made functional morphology very lively.

The terms body plan and design inevitably pop up in discussions about animal form and function. What do these terms mean in their biological contexts?

They're buzzwords. I'll discuss body plan first because it's the easiest. The body plan is basically a model, an abstraction of a particular evolutionary lineage. There is the body plan of a mammal, or the body plan of an echinoderm. It's an abstract model.

A design, on the other hand, has an engineering connotation. It means the ensemble of structures that are related to a particular function. For example, the design of the limb of a digging mammal is very different from the design of a running mammal's limb. And that would include not just the bones, but also the muscles, the ligaments, and so on. The whole ensemble is called a design.

Design is a product of functional and historical factors. We often find out that the designs we see in an organism are not perfect designs; they are not like what an engineer would come up with. We ordinarily use the word design basically from an engineering point of view, and in that sense it is a very poor term. I explain to students that biological designs change over time, usually by changes in preexisting structures. That's not what an engineer would do. Dr. Thomas Frazzetta from the University of Illinois has a wonderful saying, that "Evolution is a change while the machine is running." We probably see a lot of that in biology, and therefore we have some rather mediocre designs, but they work well enough in nature to survive.

By viewing animal form and function in this evolutionary context, does the human body make more sense? Are there medical applications of this approach, for example?

That's a very challenging question. Here's one example: Consider the evolution of the aortic arches and the heart. It would not have been possible for placental mammals to be placental mammals if we didn't inherit the lungfish design of the cardiovascular system. I tell my students, "Look, here's a ductus arteriosus and an opening between the left and right sides of the heart of the lungfishes. The ductus arteriosus can be opened or closed depending on whether the fish is breathing air or water. And that same ductus is now used during human fetal life to shunt blood, so we can be born as a placental. The medical doctor faces all kinds of cardiovascular problems that are really lungfish situations, stemming from a patent opening between the left and right sides of the heart and the continued existence of the ductus arteriosus." I try to make these kinds of connections whenever possible in my teaching. And I think students really enjoy it.

Teaching students about the evolution of various adaptations is also one way to emphasize biological diversity in a biology course. What other approaches do you take in class to expose your students to the diversity of life?

I try to illustrate adaptive radiations with many attractive slides during my lectures, using as big a diversity as I can get, sometimes taking examples from invertebrate diversifications, sometimes taking fish diversifications, sometimes plants, especially when you get into tropical ecology. Then they really start appreciating what diversity is about.

Are there reasons other than aesthetic and moral to value and preserve biological diversity?

Yes. I think it is very much in our personal interest to preserve the quality of life that we know. I usually argue that biologically diverse systems are often far more resilient to perturbations than a monoculture. The existence of the biosphere really depends on the diversity that we have. So I would say that conserving biological diversity is a matter of self-preservation.

How are human activities affecting the marine communities you study?

Well, consider Puget Sound, where I'm doing some research. In some parts it is still very good, but in other areas the habitat has been devastated by pollutants in the water. It is especially critical in areas like Puget Sound, which is an estuary, where there is little circulation.

Chesapeake Bay is another example. The worst kind of impact is probably filling in wetlands. People decide to live on the wetlands and put buildings up. That has a tremendous impact on the inshore marine communities. Around Jamaica, the main problem is overfishing. Of course, many Jamaicans are very poor and they really need the fish for food. But the fish populations have been reduced to very small size, and that has indirect impact on the coral reefs and everything else. There are many examples of human impact on marine communities.

How can ichthyologists help us sustain fish populations into the future, even as we consume these fishes for food?

Careful management on an international basis is a key element. Ichthyologists have been playing a key role in understanding life histories of fishes. When are the eggs and larvae most susceptible to death? To preserve fisheries, we must protect the spawning grounds so that we have areas where the larvae will grow. I think a good understanding of the ecology of spawning grounds and nurseries is emerging now.

Much of the harvesting of fishes, whales, and other marine organisms goes on in international waters. How effective are national and international laws and policies at conserving these marine resources, or any resources, for that matter?

I think they're not very effective right now. It's a very tough thing. In the United States, we still struggle with the concept of who owns the water and the air. Right now, we have clearly worded laws that are supposed to help protect the water and air. But the enforcement is not very good. If you were to extend such laws internationally, they would be even less effective at this time. For instance, to convince Icelanders to preserve whales is going to take a really long time. It's in their culture. They've been whalers for centuries. It's just part of their way. They love to eat pilot whale meat. So, what can you do? And there are economic complications. When I was in Iceland, they told me that up to 90% of their total income depends on export of salmon from Iceland to the United States. So if the United States stopped importing salmon to pressure Iceland to stop whaling, Iceland would go under. When it comes to developing and enforcing environmental policies and laws, there will be a lot of inertia.

You teach a very large class. In fact, most students are introduced to biology in huge classes at large colleges and universities. How can these students work their way into a more personalized situation and get hands-on research experience in a professor's laboratory? And how can we encourage that interest?

I have a system, a bit like what you're doing in your book, to expose students to enthusiastic scientists. I try to get my colleagues to give optional guest lectures about what they are doing in the lab in informal settings. If you ask a top-notch researcher to give a talk to introductory biology students, he or she will see that as a challenge and will do an incredibly good job trying to show the students that what they are doing is really fun and worthwhile. Each of those guest lecturers usually recruits students into his or her lab to do independent research or an honors thesis. Some of the guest lecturers are from Harvard Medical School. They don't have much exposure to undergraduates. And when these professors work with these students in the lab, they quickly discover that these are exciting and bright young scholars. They come to a research project without any prejudices.

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