In 1983, Phyllis Coley published a paper in Ecological Monographs reporting the results of her survey of herbivory and defense traits of rainforest tree species on the Barro Colorado Island (BCI), Panama. Based on the findings of her survey, Coley proposed a new model for the evolution of plant defenses. Thirty-three years after the paper was published, I asked Phyllis Coley about the motivation for this study, what she remembers of field work, and the current status of the model she proposed.
Citation: Coley, P. D. (1983). Herbivory and defensive characteristics of tree species in a lowland tropical forest. Ecological monographs, 53(2), 209-234.
Date of interview: Questions sent by email by 25th October 2016; responses received by email on 1st November 2016.
Hari Sridhar: This paper formed part of your PhD thesis. Could you tell us what was the motivation behind this specific piece of work, in relation to the rest of your PhD?
Phyllis Coley: This was the main part of my thesis, and it was inspired by a deadline to take my prelims and a paper I had just read by Paul Feeny. In that era, researchers were just recognizing that plant secondary metabolites were not waste products but the result of an arms race with herbivores. However, the field was still in the phase of cataloging the damaging effects of these metabolites. Feeny asked why some species invested more in defenses than others and proposed Apparency Theory, an extraordinary explanation that seemed to make sense of all the independent observations. He posited that apparent species, like oaks, would be ‘bound to be found’ by both specialist and generalist herbivores and would therefore need to invest heavily in defenses. Unapparent species, like ephemeral mustards, could escape discovery by specialists and need only invest in compounds effective against non-adapted generalists. It was a beautiful framework. He based it on two species (oaks and mustards) and I decided to test it in the tropics with 40 species.
HS: Stepping back a little, how did you get interested in the topic of herbivory, and plant-animal interactions in general, in the first place?
PC: I always liked nature, but when it came time to go to grad school, I was torn between working in municipal sewage treatment versus ecology. By almost a flip of the coin I chose ecology at the University of Chicago. I thought the tropics sounded exotic, and since I couldn’t decide if I wanted to do plants or animals, plant-herbivore interactions seemed to leave a lot open. Who knows, sewage may have been equally fascinating, but I am very happy messing about in rainforests.
HS: If you don’t mind my asking, how come your PhD supervisor(s) weren’t authors on this paper?
PC: They didn’t want to be – times have changed. I started with Robin Foster who had a very hands-off approach. So, I felt the thesis I designed was very much my own. But he gave me the confidence that it was perfectly feasible to work in the tropics. So off I went. He left academics while I was in the field, and the newly hired Doug Schemske probably felt he had no choice but to take in this orphan, warts and all. We had overlapped some on BCI [Barro Colorado Island] and he commented on how hard I worked. Poor Doug took on the responsibility of reading my painful, weekly progress on writing up my thesis. Without him, I would never have turned it into something as professional or compelling. I am very grateful to both of them for their different, but extremely valuable gifts.
HS: How did you decide to do your field work in Barro Colorado Island?
PC: I had never been to the tropics, but envisioned tenting by myself in the upper Amazon. My PhD advisor, Robin Foster, who had lots of experience in the tropics, suggested I work on BCI, the premier field station of its day. That didn’t sound so glamorous, but he was of course right. The logistics of remote tenting are enormous, and there is no one to talk to. On BCI, I was profoundly inspired by watching more senior scientists do science.
HS: Could you give us a sense of what a typical day was like during the fieldwork: where did you stay, how did you commute, did you have people to help you with fieldwork etc.?
PC: Living on BCI was a bit like summer camp, wooden dormitories with screened windows, shared bathrooms and no privacy. Most of us stayed on the island for months to years at a time, with occasional trips to town to get personal supplies. There were only about 10 people, so we got to know each other very well – like it or not. My first year on the island was one of the most wonderful, and the second year one of the worst. There were no phones and the personal computer hadn’t been invented, so it was quite isolating. I would get up every morning, head out in the woods by myself until the parrots started calling and heading to their roosting sites (about an hour before dark), which would be my alarm to start heading back too. I had thousands of plants marked in light gaps, hot, messy, ant-y places to work. I would spend all day measuring leaves with a plastic grid to quantify herbivory. Excruciatingly boring – but there were always the myriad of interactions of the rainforest that more than compensated. Once I fell in a hole and it took me hours to climb out – no one would ever have found me. Dinners were communal, overcooked and rather boring. At night I would fill in data sheets, which, back in Chicago, I would type onto cards that could be read by a mainframe computer. Then up again with the dawn chorus of howler monkeys.
Phyllis Coley on Barro Colorado Island in the 1980s with young leaves of Connarus panamensis, a vine (© not known)
HS: Do you continue to work in the study sites on BCI even today? When was the last time you visited this site? In what ways do you think the site has changed since the time you worked there for this study?
PC: I have continued to work and visit BCI over the years. It is unrecognizable: internet, hot showers, modern labs, cell phone reception, great food, a beer machine, generally more than 35 people living on the island and dozens more coming just for the day. There are even tourists. In many ways it has lost tranquility, but one can do modern biology, and I always have fascinating dinner conversations with people from all over the world.
HS: In the paper you mention a greenhouse. Could you tell us where this greenhouse was located and would you know what has become of it now?
PC: The greenhouse was plastic sheets, but there was a moat around it to keep out the leafcutter ants, so I was able to grow seedlings for an experiment. It deteriorated long ago.
HS: Where was the laboratory you mention located?
PC: The lab was actually part of my room. I had brought everything I would need, hot plate, beakers, small spectrophotometer, mortar and pestle, table-top centrifuge. When I worked with acetone, I improvised a hood: I would balance the hotplate on the toilet and put a fan in the window. It was not wildly effective at eliminating fumes, but kept one alert to make sure the hotplate did not plunge into the lidless toilet.
HS: The fiber content analysis was done in the University of Alaska Palmer Agricultural Station. Could you tell us why you chose this university to do the analysis?
PC: No idea, probably it was the cheapest.
HS: How were the figures for this paper drawn?
PC: I am amazed you asked this, but it brought back memories. Making figures was a pain! I tried two techniques – sticking black letters and lines to the paper, and using a stencil to draw/print with ink. Decidedly hand-made.
HS: Could you tell us a little more about the people you acknowledge – who they were, how you knew, how did they help etc.?
PC: Most were friends or were kind enough to read a draft. But I want to specifically mention one of them. Egbert Leigh was an eccentric Smithsonian scientist, theoretical geneticist, and resident on BCI, but he did not do field work. He called himself the ‘Toad’ and would periodically invite me up to ‘Toad Hall’, his modest apartment, for whiskey – straight of course, sometimes accompanied by cookies made by his equally eccentric wife. I was in awe and terror of him, as much of the conversation would be equations, but he was a great supporter.
HS: How long did the writing of this paper take? When and where did you do most of the writing?
PC: This is more about the evolution of my ideas: I had originally set off to Panama to ‘prove’ Paul Feeny’s Apparency Theory. By the time I had finished my fieldwork, the theory had been completely and universally accepted. But my data simply were not supporting it. That, coupled with my insecurity, meant I was thinking of dropping out on a daily basis. I eyed the sailboats passing in the canal on the way to Tahiti or other places far from my thesis and worries. Finally, I listened to my data and they actually had a much more interesting story to tell. No body was escaping discovery by herbivores, in fact you got what you paid for. Species that invested more in defense were eaten less. So if defenses worked, why weren’t all species investing in them? I decided it depended on growth rate. Slow-growing, shade-tolerant species were struggling away at 1% full sunlight, so they didn’t have the resources to replace lost leaves. Thus the optimal strategy was to protect them. In contrast, fast-growing pioneers adapted to high light maximized growth by not investing in defenses and tolerating herbivory. It was with trepidation that I presented these results at the Ecological Society Meeting soon after returning from Panama. My slides were in backwards, I was painfully shy, so to give a talk in public was torture. And worse, I knew everyone believed in Apparency Theory (except me). Or so I thought. Afterwards two bearded guys, John Bryant and Terry Chapin, came rushing up saying they saw the same thing with hares and twigs in Alaska. Many scribbled cocktail napkins later, my confidence and enthusiasm were rekindled, and we decided to write a paper together (Science 1985).
HS: Did this paper have a relatively smooth ride through peer-review? Was Ecological Monographs the first place this was submitted to?
PC: As it was a very long paper, I think Ecol. Mongr. was the only option. And it had a smooth ride, much smoother than a lot of my more recent papers!
HS: What kind of attention did this paper receive when it was published?
PC: Frankly I don’t remember. But I do remember arguing against Apparency Theory, probably like an annoying yappy dog, but I felt initially as if no one were listening. At the time, Paul Feeny, who was a famous professor at Cornell, could have squashed me and my career. Instead, he welcomed discussions, treated me with respect, and was a perfect gentleman and true scientist. He liked challenges and cared about the ideas and not his ego. He even wrote me letters of recommendation. I have tried to follow his example ever since.
HS: What kind of impact did this paper have on your career and the future course of your research?
PC: The fact that the paper is highly cited was or course very helpful. It also laid the groundwork for my 1985 Science paper, which may have reached a broader audience and became known as the Resource Availability Theory. Now this is widely accepted.
HS: Today, 33 years after it was published, would you say that the main findings still hold true, more-or-less?
PC: Yes, I think so.
HS: If you were to redo this study today, would you do anything differently, given the advances in technology, theory, statistical techniques etc.?
PC: I think the story might not be that different, but today our lab has a UPLC Mass Spec and advances in metabolomics which allow one to bring a much more detailed view of secondary metabolites.
HS: This paper has been cited over 1300 times. At the time of the study, did you anticipate at all that it would have such a big impact?
PC: Good heavens no.
HS: Would you know what is it mostly cited for?
PC: Although I think it was read initially, I am sure most of the people who cite it now haven’t actually read it.
HS: You say “I therefore suggest that intraspecific variance and skewness in herbivory among individuals be used as indices for quantifying the extent to which a population is “escaping’ damage from herbivores”. To what extent do you think these indices have been adopted?
PC: I think not at all!
HS: Could you reflect on the “success” of the model you proposed, as an alternative to the Apparency model, in the years since the paper was published?
PC: As with most things, there is a bit of truth everywhere. I think Resource Availability is still a more robust explanation for why plant species invest to different degrees in defenses. But it seems not to explain well the reasons behind investing in tannins versus metabolites that turn over more quickly, such as monoterpenes or alkaloids. Apparency had a different explanation based on effectiveness for generalist versus specialist herbivores, and it seems not to have held up either. However, temporal or spatial escape probably is a real phenomenon that will influence both ecological and evolutionary trajectories.
HS: Have you ever read this paper after it was published? If yes, in what context?
PC: Not for a long time
HS: Would you count this paper as a favorite, among all the papers you have written?
PC: It was very important for helping me see that I had a path as a scientist. However I would say that the paper we just submitted, also on plant-herbivore interactions in the tropics, is my favorite. Fingers crossed.
HS: What would you say to a student who is about to read this paper today? What should he or she take away from this paper written 33 years ago? Would you add any caveats?
PC: I can’t really remember the paper, but I will say “Listen to your data”. It helps you think outside the box.
Excellent work you are doing Sir. new insights we are getting. And especially your questions to the authors are unparallel.