Reflections on Papers Past: Revisiting Estes et al. 1998

by Hari Sridhar

In 1998, James EstesTim TinkerTerrie Williams and Dan Doak published paper in Science providing evidence to suggest that killer whales were behind the sudden declines in sea otter populations in western Alaska in the 1990s. Estes and colleagues also showed in this paper that the otter decline had, in turn, led to an increase in sea urchin numbers and consequent deforestation of kelp forests. Eighteen years after the paper was published, I spoke to James Estes about the observations that motivated this study and what we have learnt since about the killer whale’s role in this system.

Citation: Estes, J. A., Tinker, M. T., Williams, T. M., & Doak, D. F. (1998). Killer whale predation on sea otters linking oceanic and nearshore ecosystems. Science 282: 473-476.

Date of interview: 22nd July 2016 (on Skype)


James Estes at Attu Island, Alaska (© James Estes)

Hari Sridhar: Would you consider this paper a turning point in your career? The reason I ask is because this was your first paper on a whale species, and subsequent to this you have done a few more. Would you say this paper had a strong impact on your research trajectory?

JE: These discoveries certainly influenced my career trajectory. It wasn’t so much just the paper, but also the information, observations and research that lead up to the writing of that paper. This may be a matter of interest to you. Initially, I was reluctant to even submit the paper. And that was because, in contrast with everything I had done in my career prior to that time – I actually started field research in that system in 1970 and this paper was published almost thirty years later – which was forward-looking and question-oriented, this killer whale stuff was very retrospective. In other words, there was absolutely no expectation of these sort of things happening. It was the accumulation of these unexpected observations that led to the retrospective analysis, which was an effort to try to sort through what we thought was going on, what the evidence was, and so on and so forth. So I felt very uncomfortable about it, and it was only because of, mostly, the reaction of colleagues that it was an interesting story and their urging that it should be submitted, that we finally went forward with it.

HS: What were the observations that led to this paper? When did you first suspect that killer whales might be responsible for the decline of sea otters?

JE: Well, actually, killer whales weren’t part of my view of what was going on, initially. It all started in the early 1990s when I began a project to study the life history and behaviour of sea otters at Amchitka Island. Sea otters are apex predators, the population at Amchitka Island was thought to be at carrying capacity, and the broader goal of our study was to describe and understand the life-history patterns and behaviour of an apex carnivore at carrying capacity.  That is why we went back out to Amchitka Island at that time. We had quite a large number of hypotheses about what we should see, and we were trying to test them rigorously by contrasting data from Amchitka Island, where otters were thought to be at or around carrying capacity – they had been in my mind for decades – with a nearby island – Shemya – where they had recently become recolonized. We wanted to contrast body condition and foraging behaviour and reproductive success and mortality and so on, between those two circumstances. When we did the work at Amchitka, nothing fell into place. I mean, none of the expectations were met. So, for instance, I had expected to find a lot of dead animals on the beach. I didn’t find any. I expected to find animals that were in relatively poor body condition, because of competition for food in a population around carrying capacity. The data simply didn’t show that. I expected the otters to spend a lot of time feeding. They didn’t, they spent much less time feeding than I thought they should. And all of these other things. So when we finished the study at Amchitka – I think it was around 2004-2005 – I was completely befuddled. I just did not understand what was going on. But very fortuitously, we had the opportunity to continue the work at Adak Island, which was a place that was fairly similar to Amchitka, in terms of the history and status of its sea otter population.  It was during the time of that work at Adak that we started to see that the otter population was not stable at or around carrying capacity but in fact was declining and to think that killer whales might be an important part of it.  The time series of population surveys had progressed long enough by about 1995-96 that there was no question about the decline. But we didn’t understand why. And then, over the course of those several years, we had seen a lot of killer whales and several attacks on otters. That was very much in contrast with anything we had ever seen up until the early 1990s. To that point we had rarely seen killer whales, and never seen them attack sea otters. And so those observations, altogether, were what led to the suspicion –an emerging hypothesis – that killer whale predation was driving the otter population downward.

HS: How did the four authors who wrote this paper come together? What did each bring to the paper?

JE: There was myself, Tim Tinker, Terrie Williams and Dan Doak. Tim Tinker was working for me as a field technician at the time. He spent some time at Amchitka and then ran the field program at Adak. Tim was in the field at Adak throughout the year. In addition, we had volunteers who were working under his direction. I was out there mostly during the summers, because I was teaching and so on at other times, but Tim was in the field all the time. That was his role. Then, as we became more interested in why the otter population was declining and started analysing the data, we felt that we needed two other areas of expertise. One was somebody who could do demographic modelling, and so we invited Dan Doak to join us. Dan was a faculty member at UC Santa Cruz at the time. And then we felt we needed somebody who knew something about marine mammal energetics, to understand how much killer whales eat and assimilate and that sort of thing. Energetics became an important part of our conceptualisation of the modelling we wanted to do. That was Terrie Williams’ job. That’s how the four of us came together on the paper.


James Estes (L) and Tim Tinker (R) (© James Estes)

HS: Did the four of you ever meet as a group, or was it all done remotely over phone and email?

JE: No, we often met as a group because we were all at Santa Cruz. By the time we wrote that paper, Tim Tinker had come back to Santa Cruz and had joined my lab as a graduate student. And both Doak and Williams were faculty members at Santa Cruz, so all four of us met and talked frequently.

HS: Do you remember how long the writing took?

JE: It is hard to say because the paper took form though various iterations. It didn’t take very long to write the initial draft, probably a couple of days, once we had our ideas, analyses, and figures together. But then we went through quite a large number of iterations, which probably took three or four additional months. When the paper was originally submitted to Science– which was probably in 1997, I am not sure exactly – it was rejected without review. At that time, I had intended to just let it go, but another colleague of mine at Santa Cruz by the name of Bruce Lyon, who is a behavioural ecologist, changed my mind. I happened to give a lecture to his class about this work. Bruce thought it was interesting and asked me where it would be submitted at the end of my lecture. I told him what had happened with Science and he urged me to challenge the decision, because he felt it was very important work. I had him look at the paper, he made a couple of suggestions, and I resubmitted the paper with a letter requesting that they re-evaluate it. And they reviewed and accepted it.

HS: Did you do most of the writing for this paper?

JE: I did most of the writing, Tim and I did much of the analysis, Dan Doak did the modelling work that involved figuring out how many mortality events occurred and that sort of thing and Terrie did a lot of the energetics research. She determined the calorific value of otters, the metabolic and assimilation rates of killer whales, and that sort of thing. So yeah, I did most of the initial writing, but the others did a lot of follow up and provided important details.

HS: At the time it was published, did it attract a lot of attention? Were the findings considered controversial then?

JE: No, I don’t think the findings were controversial, at least no one challenged any of the results in print at that time. I know that there were people who were skeptical, based on written exchanges and verbal discussions I had with them. And I thought that was fine, because the paper was a sweeping interpretation, and certainly was not an experimental study. Yes, there was a tremendous amount of media interest in the paper. I spent weeks talking on the phone to people in the media about the paper.

HS: What do you think was the main reason for the interest – was it the system itself or was it the killer whales?

JE: I think the main reason for media interest was because of the players–killer whales and sea otters. It wasn’t so much the conceptual part of it that interested the media. I think it was the idea that these very charismatic species were interacting with one another in seemingly such a bizarre manner. But there also was the perception of significant ecological impact. People understood that not only were killer whales eating sea otters but that this was having a big impact on the ecosystem. So I think those things together—the players and their interactions–were probably what attracted so much interest and attention. The question of how we made the discovery came up frequently in talking to journalists and other people about the work.

HS: Today, 18 years after the paper was published, would you say the main conclusions still hold true, more-or-less?

JE: In my opinion yes. I think everything that we have done and seen subsequently has supported the initial interpretation. I would say there have been no qualitatively important breakthroughs, or new information, one way or the other. But there has been some quibbling. There was a paper published – maybe three or four or five years ago now – in Mammal Review that criticized our work. We were never invited to respond to it, but we submitted a rejoinder response anyway, which was not accepted. That was a dark corner. I don’t know if you have seen that paper, but you should read it. It’s by Katie Kuker and Lance Barrett-Lennard.

HS: In your paper you draw a picture of the scenario at that time and how it might have come up. Then you say “Parts of this scenario are well documented, others are more speculative and still others have yet to be evaluated”. Do we have a more complete picture now?

JE: Somewhat. The conclusion that the otters declined is unequivocal. I think the conclusion that there was a radical phase-shift in the kelp forest system that was caused by the loss of the otters also is unequivocal. We’ve seen this over and over in different settings, and it happened with the loss of the otters out there. We had very good documentation of the kelp forest ecosystem and those data are summarized in our Science paper. I think the conclusion that it was caused by killer whales will always be somewhat uncertain, just because of the nature of the data. I think the evidence is quite strong but certainly not definitive. At the time, and if you read the paper carefully, you will see that we speculated that the decline of Stellar sea lions during the 1980s was what prompted the killer whales to start feeding on sea otters. And I had imagined at that time, mostly because this was the conventional wisdom, that the decline in Stellar sea lions was a consequence of some food related problem, either because of an oceanic regime shift or because of fisheries or some combination of those two things. I now think that interpretation was wrong. I didn’t realise it at the time, but subsequent evidence for food limitation in the sea lions is counter-indicated. The weight of evidence suggests that, in fact, the sea lions had lots of food. And so I believe that the sea lion decline and the otter decline are linked, and are probably linked in the way we had initially imagined, which is that the sea lion decline led to the sea otter decline. But the cause of the sea lion decline I now see as being fundamentally different from what I had thought at that time. I think the current evidence more strongly suggests that the killer whales were the cause of both declines. I didn’t recognise that at the time.

HS: Have these areas changed since you worked there for the study? What’s happened to the otter population?

JE:  Nothing much. At the time that paper was published, the sea otter populations had declined by about an order of magnitude. They continued to decline, and otters on some of the smaller islands in the Aleutian became extinct. The present densities are holding more or less constant at very low levels overall. There is no obvious trend in any of the survey data over the last decade or so. We now have fairly long time-series of abundance of counts from surveys on different islands from the early 1990s right up to the present. What all of those data suggest is that the population has declined by 95-98 % in most places, or at least to 95-98% below carrying capacity, and that it has remained relatively constant to the present. I wasn’t out there this summer, but I was there the year before, and then the numbers and such were as I have described.

HS: Do you continue to do research in these areas?

JE: Yes, I continue to do some work out there. Mostly it’s monitoring work. I am 70 now, I had an ear injury, and so I’m not diving any more. And a lot of the research requires diving. My students, who now work in different places, are continuing to do research out there. We are continuing to monitor otter populations. There are numerous sites where we are monitoring both kelp forests and the otters, so we continue to do that as opportunity and funding permit. I will be going back again next summer to help with another project. But most of the work that I have been doing since the early 2000s has focused on related issues. Not so much on the killer whale business, but on different parts of the kelp forest ecosystem. We are currently finishing up a 3 year study of the system’s historical ecology, as it’s recorded in the growth of long-lived encrusting coralline algae. We’ve been looking at things like ocean acidification and how that interacts with kelp, and issues of that sort.

HS: In the paper you talk about Clam Lagoon as being “uniquely inaccessible to killer whales”. Why is that?

JE: Clam Lagoon is a place that was created by a receding glacier. The moraine formed the barrier between the lagoon and the outer ocean, where the killer whales are. The water between Clam Lagoon and the open sea breached at some point in the past, so there’s a narrow, shallow connection between the outer ocean and Clam Lagoon. Clam Lagoon is quite large, about two miles long by a mile wide, and it supports a population of roughly a hundred otters, and that number of animals has remained more or less constant from the time we began working on Adak in the mid-1990s. So Clam Lagoon was created fortuitously by this geological event, and the connection between Clam Lagoon and the open sea is too shallow for killer whales. They just don’t go in there.

HS: In one of the notes to the paper you say that your research team spent 21,677 person hours in field. That is a lot of field time! Could you give us a sense of over what period this was, and how many people it involved?

JE: Well, I had been working in the Aleutians for more than 25 years at the time. And we were in the field every day from morning till evening. I usually worked with a team of four people during the later years. Early on, during the 70s and up to the early 80s, it was usually just two of us, and then after that it was commonly four. So, there were a lot of people, over a lot of days, over a lot of years, and when you sum it all up, the number of person hours in the field becomes  very large.

HS: In the Acknowledgements, you talk “about a contract from the U.S Navy”. What was that for?

JE: I had mentioned to you before that I worked at Amchitka in the early 90s, when we were looking at the life history and behaviour of otters. That work was funded by the US National Science Foundation. After I left Amchitka, the Navy supported a follow up study at Adak. What happened actually was that, as I was leaving Amchitka, as we were wrapping up the study at Amchitka in 1993 or 94, I happened to be talking with Dan Boone, who was the manager of the Aleutian Islands Unit of the Alaska Maritime National Wildlife Refuge. He approached me and said the military – both the Navy and the US Air Force – were interested in having work done on sea otters at their respective military bases. Adak was a naval base and Shemya Island, where we worked some years later, was an Air Force base. There was a military programme, called the Legacy programme, which was for doing wildlife and ecological research on US military bases. Some of that Legacy money had gone to those particular sites and the Aleutians Refuge was asked to advise the military on what to do. That’s how I got involved with it.

HS: Were the people who you thank for field assistance – C. Dominick, B. Konar, J. Meehan, K. Miles and J. Stewart –all students?

JE: C. Dominick was a student helper who worked with us at Adak. Brenda Konar was one of my graduate students, who at the time this work was done was just finishing her dissertation research at Shemya Island. Brenda helped me with the diving work. J. Meehan was an employee of the Fish and Wildlife Service, who helped us at Adak. K. Miles was an employee of the US Geological Survey, also my employer at the time, and he came out to the Aleutians to help me with diving on various occasions. Julie Stewartis now Tim Tinker’s spouse, but she was his partner at the time, and they worked together during the 1995-95 period on Adak. She was also a trained field biologist and helped Tim with the fieldwork.

HS: Could you also tell us about the people you thank for comments on the manuscript?

JE: Ken Clifton was a post-doc. at Santa Cruz at the time. He is now, and for a long time has been, a faculty member at Lewis & Clark College in Portland, Oregon. Don Croll is a fellow faculty member at the University of California (UC), Santa Cruz. Eric Danner was one of my graduate students at the time. He worked with us in the Aleutians. He is currently an employee of the National Oceanic and Atmospheric Administration (NOAA) and works at the Santa Cruz Fisheries lab. Laurel Fox is another fellow faculty member, a terrestrial plant ecologist from UC, Santa Cruz. Bruce Lyon is also a fellow faculty member at UC Santa Cruz. Lyon is the person who I referred to earlier, whose class I was speaking to, who urged me to resubmit the paper to ScienceRick Ostfeld is an ecologist I met decades ago, when he was an undergraduate student at the UC Santa Cruz. We’ve remained close over the years. He is a research ecologist, and has been for a long time, with the Cary Institute for Ecosystem Studies in New York. Mary Power is a professor at UC, Berkeley. Alan Springer is a professor at the University of Alaska. Springer and I, subsequently, did some work together and published a follow-up paper in PNAS, which you may have read, that linked all of this stuff to whaling.

HS: Towards the end of your paper you talk about intersystem linkages becoming increasing well-known at that time. Subsequent to your paper, do you get the sense that people went out and looked for other such linkages?

JE: It’s hard to know. That was one of the big messages, or one of the revelations, that came to my mind in thinking about what it all meant. I would like to think that our paper impacted people in that way. The results certainly influenced my thinking. It’s hard to know how other people have thought about these things. A few years before our paper was published, Gary Polis and several others published an Annual Review on subsidized ecosystems. That paper explained how ecosystems are linked together, and most of the case studied that Polis talked about were connections between land and sea – nutrient subsidies from the ocean to land and so on and so forth. The Polis paper motivated me to start thinking about these issues. Before he published that paper, I think most people imagined that adjacent ecosystems function into themselves, more or less separately from one another. The intriguing feature of our study was the idea that linkages between ecosystems resulted not only from material and energy flux, but from the movement of individuals and species, and that even relatively rare things like killer whales could potentially have big effects. I don’t know how much that idea has trickled down to other people. I think it probably has had some impact on the way people think about how nature works.

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 18 years after it was published?

JE: Well, let me think a little bit about that. I think maybe three or four things. One is the serendipitous nature of the way the science was done. That’s really the theme of my recent book. When you read that you will see that that’s really what I’m writing about. This was not a question-driven or hypothesis-driven study. It was a retrospective study and very much based on, what I call, serendipitous events. Things that happened that we were perhaps lucky to see. The second point I would make is more theoretical and has to do with food web structure and dynamics–the idea that effective food chain length has strong impacts on the nature of plant-herbivore interactions. So this is really a follow-on from the ideas of Stephen Fretwell- that even-numbered food chains cause strong plant-herbivore interactions and odd-numbered effective food chains cause weak plant-herbivore interactions. Fretwell published two papers –one was in 1977 and the other was in 1987. The ‘87 paper was in Oikos. That was where he really proposed his theory. What we have in this particular study is documentation of the dynamics of plant-herbivore interactions in a food chain that is effectively two trophic levels – that’s just the urchin and kelp – three trophic levels when otters are added in, and four trophic levels when the killer whales become part of it. So our paper supports Fretwell’s hypothesis. Another important message is that what one discovers about nature may not be at all what one was expecting to see and learn. And I don’t know how strongly that comes through, but you know it took us several years to open our minds to the possibility that these things were going on, even though the evidence was there earlier that there were major changes happening. My belief system about the way that system was put together, and the fact that I thought the sea otter population was at carrying capacity, really prevented me from seeing the truth till later. I don’t know if that comes through from the paper. It definitely is a point of emphasis in my book. Finally, the idea that large predators can strongly influence ecosystem structure and dynamics. Those are the main points.

HS: In the last sentence of the paper you say “These points emphasize the potential significance of large-scale ecological events and the consequent need for large-scale approaches in ecological research”. Could you tell us what exactly you meant by large-scale approaches?

JE: Well, what I mean is this. I think a lot of marine ecology and coastal marine ecology especially has been very experimental, necessarily done at very small spatial scales. By small spatial scales I mean at the level of metres to tens of metres to hundreds of square metres, in some cases. Those are the sizes of the experimental units. The point I think was that, studies that are done at that scale, that are done in order to achieve experimental rigor – through manipulation and replication and so on – are necessarily going to be constrained to species whose behaviour,  life histories and spatial ecologies occur at those small scales. The time scales over which these experiments are done is also usually fairly short—usually no more than a few years. And the point I was attempting to make was that we have seen at least the hints of processes in this system that occur at much larger spatial and temporal scales. So the effect of otters was seen by comparing islands with and without otters. We simply can’t see that effect by looking at one particular island. It requires looking at islands that are separated by often times hundreds of kilometres to see that effect. And the impact of killer whales occurred at an even larger scale. It occurred at the scale of an entire ocean basin, or at least part of an entire ocean basin. So I was arguing that we need to be looking at patterns of variation in nature that occur over these very large scales to see these kinds of processes. I’m still not at all sure that people get this. Does that make sense to you? I mean, did that come across?

HS: Yes, it does.

HS: Would you count this paper as one of your favourites, among all the papers you have published?

JE: Yeah, it’s one of them certainly. It was fun to write, I think it was an important paper, and it generated a lot of interest and attention. Is it my very favourite? I don’t know. The first paper I ever published in 1974, which was on the sea otter kelp trophic cascade, is to me, personally, the most important paper that I ever wrote. I’ve written a couple of other papers that I would say were comparable. I’ve written papers that I think were good papers, and I think this was a good paper given the questions and the nature of the evidence. But from the perspective of an experimental ecologist it was probably not a good paper. It’s not experimental ecology. But I liked it because I felt like we were able to make a reasonably compelling argument for the cause of this amazing pattern that we saw, and I feel good about both the philosophical perspective and the intellectual infrastructure that went into disentangling all this stuff. So yes, in that sense it was great fun.