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  • Post date: 1 year 6 months ago
    Citation for this post: BibTeX | RIS

    In 2002, , and published in PNAS showing how the introduction of pigs had reshaped an island’s foodweb and caused the decline of an endemic fox. Fourteen years after the study was published, I spoke to Gary Roemer about the making of this paper, and what has happened to the foodweb since.

     (Interview conducted via Skype on 21 July 2016)

     Citation: Roemer, G. W., Donlan, C. J., & Courchamp, F. (2002). Golden eagles, feral pigs, and insular carnivores: how exotic species turn native predators into prey. Proceedings of the National Academy of Sciences 99: 791-796.


    Hari Sridhar: What motivated you to do this study?

    Gary Roemer: Well, actually, it was serendipitous. I went out to the islands to study the behavioural ecology and genetic structure of . And while I was there, I started to see some mortalities of foxes. I had worked with bald eagles in the past, and had figured that golden eagles, which were irregular visitors to the island, were taking foxes every now and then. And then I started seeing a steep decline in the foxes while I was there, so I just happened to be at the right place, at the right time, to be able to identify what was going on.


    HS: So your PhD, to start with, didn’t have anything to do with this set of interactions? It was focused only on the island fox?

    GR: Exactly. It was going to be a study on their social organisation, dispersal and genetic patterns, foraging ecology etc., you know, sort of an autecological view of the island fox. And all this happened while I was there.


    HS: How did this group of three authors come together?

    GR: Well, I had published in Animal Conservation based on this. I had used in that paper.  And then - I think it was either 2000 or 2001, I have got to look back - I gave a presentation on that work at the in Missoula. Josh came up after the talk and, you know, started rapping with me and we kind of hit it off and became friends. And then a little bit later I was talking to him over the phone about an aspect of the research that I wanted to try and get a handle on, which was to evaluate the food habits of the golden eagles. Josh said: “well, we could use stable isotopes to get at a broad-scale look at their food habits”. So then, he and I started conversing about that and felt Franck was a better modeller than either one of us, so we asked him to be involved. That’s how the team came together.

     HS: Did you do all the fieldwork and the data collection?

    GR: Yeah, that’s correct, myself and various technicians. Josh came out once to help me collect tissue samples from feral pigs.


    HS: How did you build upon the Animal Conservation paper for this paper? Was it through the modelling that Franck Courchamp did?

    GR: Yes. There was some modelling in the Animal Conservation paper as well, but the model was developed further here. The structure of the models were similar, but the model in the PNAS paper was more elaborate, and we included additional parameters that would make the model more realistic. We also included , which were a competitor of the fox. Not just the pigs. The original model in the Animal Conservation paper was just trying to show that pigs were probably one of the more important prey animals that was driving this interaction.  Then, the stable isotope information was also helpful in determining certain species interaction factors that we used in the PNAS model.


    HS: Did the collaboration for this paper start after the Animal Conservation paper was published?

    GR: Yes, I think the Animal Conservation paper was already published or at least in review. I had already put that paper together, because that’s also what my presentation at the Society for Conservation Biology meeting was based on. And as you know, the whole process takes a long time, so that process had been ongoing for probably a couple of years before we got the PNAS paper together.


    HS: How did the collaboration actually work? Did the three of you ever meet? Was it mostly over email?

    GR: Yeah, it was mostly over email and on Skype a couple of occasions. There were a couple of phone calls as well. Josh and I got together more frequently, but Franck was over in France, so with him it was always remotely. As a matter of fact, I had never met Franck till about - I am trying to remember the year - I think it was 2004 or 2005 at the Society for Conservation Biology meeting down in Brazil.


    HS: Was most of the writing for this paper done by you?

    GR: Yes, Josh and I were the principal writers.


    HS: Do you remember how long the writing took?

    GR: Originally, we put a paper together for Science. That was a shorter version but that didn’t make it. And then we communicated with . I don’t know if you are familiar with Dr. Estes; he just wrote a book called about his experiences in biology. But anyway, Jim suggested that we submit to PNAS and offered to help us communicate it, if you will.

    The whole process went pretty quickly actually. I would say within six months we had contacted each other, done the analysis, written the paper, got bounced, talked to Jim - it was all relatively quick. We submitted the original manuscript on August 11, 2001, received comments back and submitted a revision on October 16, 2001, and the paper was published on January 22, 2002.


    HS: But on the paper it says this was a direct submission to PNAS?

    GR: What happened was Jim communicated with who is a Member; Dr. Mooney gave us some more advice on how to craft the paper. We had submitted the paper directly, but Jim had suggested that Dr. Mooney take a look at the paper because he thought it was a really nice study and that Dr. Mooney could give us some good advice. Jim also did a real nice job helping us edit the paper and giving us suggestions on how to improve it.


    HS: The paper is full of really interesting natural history information. Was all that already known or did it come from your PhD?

    GR: Well, certainly for the foxes, a lot of that was from my PhD work as well as work that I had done previously. I had been working with foxes since 1988. About the eagle and the skunk, a lot of that was just from my experiences working with the particular species or related species. I guess I would consider myself more of a scientific naturalist, in general. Natural history is important to me.


    HS: Yes, that is so evident. The paper really stands out because of the natural history in it. Did you have help in field or did you do most of this work on your own?

    GR: No, I always had one technician at any time during the project. There were various technicians that worked on the project, and one or another one of them worked with me during the entire project, they did everything that I did.  The technicians included my cousin, Tom Roemer; a really good friend, ; Rachel Wolstenholme, Dr. , and Dr. Jeff Howarth. However, Paula, Deb and Jeff were not doctors at the time! I taught most of them how to handle the foxes, how to track the foxes etc. Except for Paula, who had as much or more experience than I, primarily with Arctic foxes. So, we worked as a 2-person team.


    HS: Was most of your work on ?

    GR: Well, my dissertation focused on Santa Cruz, but I worked on all the islands where there were foxes, from 1988 to about 2001. That was the last time I was in the field working on foxes specifically.


    HS: You cite a personal communication from , for some information from Santa Rosa. Was T. Coonan also working on foxes on other islands?

    GR: Yeah, so what happened was, originally I was going to be doing my work on , and I was partially funded by the National Park Service. But because of political situations on Santa Rosa Island the park superintendent sort of nixed that project. I had applied for money and got funding through the park service to do the work, Coonan was one of the park service personnel who really championed the project. He convinced his administration to allow the transfer of the funds to Santa Cruz Island, because the work on Santa Cruz was germane to the rest of the island fox populations. And at that time, the National Park Service oversaw , Santa Rosa Island and about a third of Santa Cruz Island. So when I started the project on Santa Cruz, I trained two biologists from the National Park Service - Tim Coonan and to start a grid-based mark-recapture analysis on San Miguel Island. Shortly after beginning my work on Santa Cruz, I started seeing declines in the fox population there, this trend was based on population estimates derived from two grids and various transects where we were trapping foxes. So my estimates of population size were declining, and then of course I was also seeing all these mortalities with radio-collared foxes. Over on San Miguel Island, where they were running three trapping grids, they started to see declines in foxes there as well. But we had no information from Santa Rosa Island. And so I convinced Tim to send me, and another colleague and NPS employee, Keith Rutz and a colleague of mine Chris Starbird, the three of us went to Santa Rosa Island to basically do a sort of reconnaissance mission; a short trapping mission to see what we might find there. And when we went there we only caught nine foxes over the course of about 80 trap nights. And normally, if the fox population had been very abundant, over 80 trap nights, we would have caught anywhere from about 20 – 40 animals. And we had put the transects in a variety of different places around the island over the course of a few days. We put 10 traps here and 10 traps there and we moved them around and then we looked for sign and we found hardly any sign and so we convinced the park that the fox population on Santa Rosa Island had probably declined as well. When the Park Service finally started the captive breeding program on Santa Rosa Island, they only caught 15 individuals to start it. So that’s where that information was relevant.


    HS: Did the paper attract a lot of attention when published?

    GR: Oh yeah it did. It was recognised as a really interesting study with respect to how exotic species can cause native species endangerment, and one that uncovered a mechanism that was contributing to a decline of an endemic species. I got a lot of calls and there was some press and I have a folder full of things about where it was showcased in different articles. Then I had a number of requests for speaking engagements, especially at universities. So yes, it created quite a buzz. It was kind of neat you know. I mean it was sad for the foxes, but it was a neat piece of science and it jump-started my career.


    HS: When I emailed you requesting an interview you said your paper was “more infamous than famous”. Why was that?

    GR: [Laughs] Well, I think because at the time maybe I wasn’t as politically astute as maybe I am now, although some would say I haven’t changed (!), and it resulted eventually in me kind of being blackballed by the National Park Service. And I can send you a couple of other papers that sort of outline the scenario that unfolded with this study. They were written by Josh and I, and we published them in Endangered Species Update (, ). And maybe after I send you those if you want to have another discussion we can, but basically I really upset the park service with the things that I did to try to save the foxes.


    HS: What kind of impact did this paper have on your career and the future course of your research?

    GR: It got me my job, for sure. I hope the quality of the science was important, but certainly, I think, the publicity and whatnot helped me get my job. At the time in 2001, when I had the interview here at New Mexico State University, I presented that work, and I think that helped solidify the offer for my position.

    In answer to the second part of your question, well, no, I wouldn’t say that. Certainly, I was interested in apparent competition and the effects of predation, but once I got here to New Mexico State, I started doing other things that were related to population demography of south-western taxa. So it really didn’t, although it probably did inform me to some degree .


    HS: You haven’t worked on this particular system after this paper?

    GR: Essentially, well I did fieldwork until 2001, and we have published some other papers since then that were related to that. I don’t know if you are familiar with . That was a real nice piece of work, I was really happy to be involved in that. So there were a few things that came after, but after my fieldwork sort of stopped in 2001, anything that I published afterward utilized data that I had collected in the past. I am not actively working with island foxes now.


    HS: Did this paper have an impact in terms of how people think about introduced species and apparent competition. Have people gone out and looked for more examples?

    GR: Yes, I think it did or perhaps I am just noticing studies that are similar. My paper has been fairly widely cited. You know was the original individual that came up with . I think that because my study dealt with some charismatic species, it helped to elevate the awareness of this mechanism, especially with respect to indirect impacts wrought by introduced species. But certainly, the idea of apparent competition had been around for quite sometime. And, you know, Franck’s work sort of recoined it - he used a different term for apparent competition in his paper – hyperpredation. I think Franck’s work originally tied the mechanism to introduced species, that’s sort of what alerted me to the potential interaction, because when I read , that sort of was a corollary for me with regard to what was going on with pigs, eagles and foxes. I think our paper may have at least made other scientists and managers a little bit more aware of the potential role of that process, especially with respect to introduced species.


    HS: Do you have a sense of what this paper mostly gets cited for?

    GR: In general, as an example of how introduced species can influence native species, in more of an indirect way rather than a direct way.


    HS: In general, would you say the citations are appropriate, i.e. for things that are in the paper?

    GR: Yes, with respect to this whole idea of how apparent competition is a process that’s important for us to explore in the decline of native species.


    HS: Did the study lead to conservation action, e.g. the translocations?

    GR: Oh yes, the study itself formed the biological underpinnings for the recovery actions implemented by both the National Park Service and The Nature Conservancy to start to restore the islands. As a matter of fact, this year, , at least three of the four subspecies were delisted - the three northern island subspecies where apparent competition had occurred - were removed from the Endangered Species Act (ESA). Also, one of the subspecies on , which had declined as a consequence of a canine distemper outbreak, is going to be downgraded from Endangered to Threatened. They are showcasing this as an ESA success story, because it’s the fastest recovery of an endangered mammal in the history of the ESA.


    HS: In the model you built you made some assumptions about the system? Have those assumptions been shown to be true by future work? Is there research work happening on this system by other people?

    GR: Well, the other main piece of work that came out was the work by Dr. Vicky Bakker, which we did collaboratively. . I don’t know if you have a copy of that; I can send it to you. But that was a really in-depth study, and there’s a bunch of natural history in there as well, which I had contributed to. That paper basically confirmed what we did in the PNAS and Animal Conservation papers, but extended our earlier work via a population viability analysis (PVA) that identified population drivers, predicted extinction risk, and also suggested monitoring strategies. And all of this, in part, contributed to the process that the Park Service, and then eventually the United States Fish and Wildlife Service (USFWS) in conjunction with The Nature Conservancy, put together to restore the foxes. So we ended up.. I guess I should say they ended up removing pigs, translocating golden eagles, reintroducing bald eagles, captive breeding and releasing island foxes, and then establishing a monitoring programme whereby they are monitoring fox populations and also looking at causes of mortality to ensure that golden eagles don’t come back and nest on the islands again.


    HS: Is the island now free of golden eagles and pigs?

    GR: Yes. Well, there still maybe eagles that come out and visit the islands periodically.  They always used to. It wasn’t abnormal to see golden eagles on the island, especially during the non-breeding season. I guess the pigs were removed by about 2006. And then the bald eagles were reintroduced, and the bald eagle population is doing very well. They are breeding there and because they are territorial they act as a deterrent to the golden eagle. They’ll tend to keep other raptors out of their territories. So all that together was something that probably facilitated the recovery.


    HS: In the paper you say that disease is probably not a very important factor. Is that still your view? I am asking because you mentioned canine distemper a short while ago.

    GR: Well disease was important on Santa Catalina Island. But on the northern Channel Islands - that would be Santa Cruz, Santa Rosa and San Miguel – hyperpredation was responsible for the declines. On Catalina Island, which is a fair amount south, there had been an introduction of canine distemper virus, which wiped out about 3/4ths of the population. And the folks who were working there recognised what was going on, implemented a vaccination programme, a captive breeding programme, and a translocation and release programme, and recovered the fox population. So the idea that diseases can impact island fox populations is definitely real, and perhaps even more important given the fact that island foxes tend to be less genetically variable than mainland populations.


    HS: This is a minor point – you say “Foxes and skunks were live-captured on Santa Cruz Island on two grids (13 km apart) from 1993 to 1999 with a hiatus in 1994”. Can you tell us why there was a break in 1994?

    GR: On Santa Cruz specifically?

    HR: Yes.

    GR: Well, the hiatus wasn’t throughout the entire year. I am trying to remember what exactly happened there. I think what happened was that I was focusing not on the telemetry aspects but on the demography aspects, and I was unable to run the grids that particular year. I have to go back and look again to recall, but I think that’s what happened. Let me pull up the paper, but I’m pretty sure that’s where the data glitch was. Let’s see. It’s a long time since I looked at this paper. Yes, so if you look at Figure 1, you can see I don’t have any demographic data for 1994. That data is from the grids that we ran - these were mark-recapture grids - so from about mid-1993 to the end of 1995, I was doing telemetry and running these demographic grids during the summer. In 1994 I elected to not run the grids and to focus my efforts on the telemetry. I was still there doing research, but I thought that evaluating the mortality and keeping a closer eye on the foxes was more important, because the grid trapping is a considerable effort and takes at least a month’s worth of time to run.


    HS: Did the telemetry data go into the Animal Conservation paper?

    GR: Yes, it’s in there. In that paper I did some matrix population modelling, and the survivorship values come from the telemetry data. I also showed changes in survival across islands based on telemetry data. Then I have - I don’t know if you saw this one – in Journal of Zoology on the fox’s behavioural ecology, on what happens to their social organisation as individuals are killed by eagles.


    HS: You just mentioned that it was a long time since you read this paper. When was the last time you read this?

    GR: Oh geez I don’t know! It was probably a decade ago. I haven’t really looked at the paper in a while. I’m doing other things now, and I haven’t sort of used this approach per se since then. Although, I have looked at the Animal Conservation paper, in the context of some matrix population modelling stuff that I was doing, to look at what I did there and how I can do things differently.


    HS: I would like to go over the list of people you acknowledged, to find out a little more about their roles.

    GR: Sure. Let me look at it. Okay, . I believe he is still the reserve manager. The University of California has a number of reserves that are located throughout California. I think there are somewhere around 33-35 of them. And one of them is on Santa Cruz Island. These are places where both researchers and educators can go. Mostly people do field trips. They go to the island for a weekend or 10 days, something like that. But also, long-term research emanates out of these reserves. These reserves had vehicles and a place to stay, so I would stay at my remote field site for 20 days every month. I lived on the island for 2.5 years and Lyndal supported me in many ways. I can’t count the ways he helped me. Actually, Lyndal did his PhD on the foxes as well.


    HS: You have already told me how Coonan helped. What about and ?

    GR: Those were two colleagues and mentors of Josh who helped us with the isotope analysis. In particular, with making sure we were interpreting things correctly. Both of them were previously from Northern Arizona University, where Josh finished his undergraduate degree.


    HS: , who provided skunk serum samples?

    GR: He was a colleague who I had worked with on island foxes for many years. He had come out to Santa Cruz Island and sampled skunks out there, and I had helped him trap and draw blood from skunks for a genetic analysis. Subsequently, the serum samples were used in the isotope analysis.


    HS: T. Gorton, who assisted with the figures?

    GR: Yes, that was another colleague of Josh’s, who gave us some ideas on how we could improve our figures, etc. Once we had put the paper together, we had discussions with individuals before the paper was finalised, and T. Gorton gave suggestions on how we could improve the figures.


    HS: And then there are a number of people who commented on the paper.

    GR: Yes, we sent the paper out before the submission to Science, and then we sent the paper out before the PNAS submission. We tried to get as much feedback on the paper, because we definitely wanted to try and get it published in PNAS. All those individuals made valuable comments to improve the quality of the paper.


    HS: You acknowledge numerous sources of funding. Were all of these given specifically for this work?

    GR: Well it was in conjunction with my dissertation research originally. Everything supported my dissertation research. So I wouldn’t say that funding was specifically to study this interaction. Rather, the funding was for doing the ecological study of the island foxes and then this research emanated from that.


    HS: What would you say to a student who is about to read this paper today? What should he or she take away from it?

    GR: Well, first, that sometimes when you go into a study, other things may surface that you should pay attention to. In my case, I think because of my previous experience, I was able to recognise what was going on, and then because of the observations that I made while I was on the island, it sort of made me figure out what the mechanism was. I’ll just digress a bit to give you an example. We knew that eagles were killing foxes, but there was one day when I was driving into my study area, and I saw a golden eagle take off from a hillside and I noticed it had a full crop.  It had just fed. So I stopped the truck and I started scanning the hillside to see if I could see any remains. I spotted some blood and what looked like a small carcass. So I grabbed my … I didn’t grab my camera , this is where I made an error – but, anyway, I hoofed out there  - it was quite a way, it was several 100 yards  - and when I got there, I saw a piglet. The golden eagle had killed and fed on a piglet. I think that was my ‘aha’ moment. I realised that while the eagles were killing foxes, that wasn’t the only thing that was supporting the eagle population. The piglets are really important for supporting the eagle population. So, by way of advice to students, I would say that you should always be observing nature and shouldn’t be afraid to make inferences from your observations, or follow up on those inferences, even if those weren’t things you originally planned to do.

    Then the other thing I think that’s really important is to try and ground your research in ecological theory. My background is real big in natural history, and wildlife biology in general, but I found that the most interesting way to advance science, or contribute to science, is to look at how theory relates to the work that you do. Subsequent to this study, I have also tried to set up studies with specific ecological theory in mind. I am an empiricist, not a theorist, but I try to collect data that might address certain theories. I always have theory in mind.

    I guess the third thing would be: serendipity happens. Don’t ignore it, but, instead, take advantage of it.

    Finally: collaborate. You know, some people - I was certainly guilty of this when I was young as well - get proprietary with their work and they want to get fully credited for the work they do. But the work can be much richer and much better when you collaborate with folks, and then, as a consequence of that collaboration, you end up learning more and you end up becoming a better biologist, a better scientist.

    So those are probably the four things I would ask students to be aware of as they proceed along in their career.


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

    GR: Yes, it is. More recently, another paper I really like is . I thought my graduate student, myself and one of my colleagues did a really nice job there. There are a few other papers too. I really like my and also , which was published in the Journal of Zoology. I think when I look back upon my scientific career now - I still hope I have a little more to go  - I have to say that my dissertation experience was one of the most quality research experiences that I have ever had. I was living on Santa Cruz Island for 2.5 years and I was completely focused on doing field work and science.  It was just a fantastic experience for me. I really look back on that time fondly, and it certainly enabled me to have the career that I have today.






  • Post date: 1 year 6 months ago
    Citation for this post: BibTeX | RIS

    in 1980, provided experimental evidence to show that guppy color patterns represented a “shifting balance” between the effects of sexual and natural selection. Thirty-six years after the paper was published, I spoke to John Endler about his motivation for doing this work and what we have learnt about this topic since the paper was published.

     (Questions send by email on 28 July 2016; initial responses sent on 4 August 2016 and additional responses sent on 2 September 2016)

     Citation: Endler, J. A. (1980). Natural selection on color patterns in Poecilia reticulata. Evolution 34: 76-91.


    Hari Sridhar:  How did you get interested in guppies and the topic of animal colouration? 

    John Endler: Pure curiosity.  , and I thought it would be a perfect system to test my theoretical predictions, derived from my just-finished PhD thesis.  I then went on to looking at the balance between sexual selection and crypsis (difficult for predators to see) because there were predation intensity gradients going downstream, just like described.


    HS:  Today, 36 years after it was published, would you say that the main conclusions of this paper still hold true? If you were to redo this study today would you do anything differently? 

    JE: Yes, the main conclusions still hold true, and that's why it keeps being cited.  And if I were to redo it today I can’t think of anything that I would change. Of course, nowadays, we can add lots of interesting genome methods.


    HS: In the paper you say “The next step will be to measure the differential survival of color pattern classes to enquire whether or not the color patterns which are predicted to be most adaptive on the basis of background matching actually survive better than those which are mismatches to the background." Has this happened?

    JE: Yes, I've got lots of data that I'm writing up now.  (former PhD student) has more on a big collaboration with me and others on some wild populations.


    HS: You say "There are three possible and not exclusive reasons [for why there are not more species with the same degree of polymorphism as guppies]: habitat, species recognition, and automimicry." Today, do we know more about the relative importance of these factors in causing polymorphism? 

    JE: We now know a lot more about each, but not their relative importance! This is probably because most people are going molecular and neglecting the ecological reasons behind polymorphisms.


    HS:  What would you say to a student about to read this paper today?     What should he or she take away from it?

    JE: There are many more papers on the subject since then, all worth reading. Particularly good authors are , , , and . These people did, and are still doing, some lovely tests of many of my early ideas, and going considerably beyond that.


    HS: There is one intriguing sentence in the first paragraph of your     paper: "Until we know more about how and why natural selection occurs,     attempts to measure it are quixotic, and discussions of its importance     are theandric." Can you tell us a little more about this sentence and     why you decided to frame the issue in this way? 

    JE: At the time, almost all discussions and studies of natural selection just estimated it over parts of life cycles (incomplete estimates) with no understanding of why it occurred ().


    HS: Did this paper have a smooth ride through peer-review? Was Evolution the first place you submitted this paper to? How different was the final published version from the first submitted draft? 

    JE: Yes, it went through with only minor comments. Evolution was the first place I submitted it to.  But it was a genuinely pioneering paper.


    HS: When was the last time you visited the field sites where you did this study? Have these sites changed a lot since the time you worked there for this study?

    JE: In 1991, although my former Ph.D. student, David Reznick, still visits. Yes, most of the study sites have changed enormously.  In fact, what I did then couldn't be done now because many of the low predation sites, most of the medium predation sites, and all of the high predation sites have been ruined by logging, silting, or chemical fishing.  Current studies (by Reznick's group) are at low predation sites as far as possible from human disturbance.


    HS: Would you count this paper as one of your favourites among all the papers you have written? If yes, why? 

    JE: Yes, it was pioneering and produced good clear results of general interest. Also, it was the first formal study on the balance between sexual selection and predation jointly affecting sexually selected colour patterns and varying geographically with predation intensity.


  • Post date: 1 year 7 months ago
    Citation for this post: BibTeX | RIS

    In 2001, , Lawrence Lopez, Percy Nuňez, , , Gabriela Orihuela, Mailen Riveros, Rafael Ascanio, , and published in Science demonstrating a trophic cascade on predator-free islands, which were created as a result of the construction of . Fifteen years after the paper was published, I spoke to John Terborgh about the making of this paper and what’s happened on these Venezuelan islands since.

    Citation: Terborgh, J., Lopez, L., Nunez, P., Rao, M., Shahabuddin, G., Orihuela, G., Riveros, M., Ascanio, R., Adler, G.H., Lambert, T.D. and Balbas, L., 2001. Ecological meltdown in predator-free forest fragments. Science 294(5548): 1923-1926.

    Questions sent by email on 12th August 2016; responses received by email on 28th August 2016.


    Hari Sridhar: I would like to start by talking a little bit about your motivation for doing this study. In 1988, you published a short essay titled "", in which you lay out the possible consequences of the loss of top predators on lower trophic levels. In that it almost seems as if you anticipated your subsequent findings in Lago Guri. When and how did you first learn about Lago Guri, and why did you decide to work there?

    John Terborgh: I learned about Guri from a colleague, Warren Kinsey, a primatologist, who told me about his new research site in a giant hydroelectric project in Venezuela.  I hadn’t known about Guri before that. It was 1990. Later that year, I went with two graduate students and Warren to visit his camp on one of the larger islands. It was exactly what I had been looking for, for many years – a giant replicated fragmentation experiment.

    Yes, the “Big Things” commentary did anticipate some of the findings, but I had received a lot of criticism and disbelief from colleagues about the Big Things article and was anxious to find support for my interpretation in a replicated system that would not be subject to the N = 1 criticism.


    HS:  This paper has 11 authors. How did this group come together and what did the different authors bring to this study? Did all members of the group ever come together in one place at any time?

    JT: I first saw Guri in 1990 but we didn’t begin the research in earnest until 1993. The Science article was published, I believe, in 2001. By then, the project had attracted a number of PhD and Master’s students, each of whom undertook a sub-project. The Science article published a summary of results to which the 11 people had contributed. Were we ever all together in the same place? I couldn’t say, but most of us were in the field together for one or more years.


    HS: How long did the writing of this paper take place? At the time of writing this paper, did you have a particular writing routine, with regard to where and when you wrote?

    JT: Do you mean the physical act of writing? That didn’t take long. I write quickly. It might have taken me a day or two. What took much longer was compiling and analysing the data. I do most of my writing at in Peru (where I am now), but I don’t remember where I wrote the Science article.


    HS: Did this paper have a smooth-ride through peer review? Was Science the first place you submitted this paper to?

    JT: Yes, I was fortunate and it was quickly accepted.


    HS: How was this paper received on publication? Did it attract a lot of attention in academia and the popular press?

    JT: By now it has attracted nearly 1000 citations, so that suggests it did attract attention. As for the popular press, I can’t say.


    HS: Did this paper, in any way, influence your future research trajectory?

    JT: I would say that trajectory was already quite well established.


    HS: Today, 15 years after its publication, would you say that its main conclusions still hold true, more-or-less?

    JT: Definitely, as further detailed in the I published with and others more recently.


    HS: If you were to redo this study today, would you do anything differently, given the advances in technology, theory and analytical techniques?

    JT: There was something I wanted to do, but didn’t do, that would have been a clincher. That was whole island experiments, in which we removed leaf-cutter ants from some, rodents from some, and both ants and rodents from others. And, of course, there would have been untreated controls. We were starting to implement these experiments at the end of the study, but then two things happened, both beyond our control. First, there was a 3-year drought that brought the water level in Lago Guri down 26 meters. Yes, that’s 26 meters. This exposed many km2 of lake bed and effectively connected all the experimental islands to each other and the mainland. The last year we were there – 2003 - we found 6 different predator species on islands where we had not previously seen any predators at all, over a 13-year time span. This was convincing evidence that, in fact, the islands were predator-free during the main period of our research. Second, came in as President of Venezuela in 1999 and was cracking down on foreigners, especially Americans. There was no way we could have continued the project under his government.


    HS: In the paper you say "We expect that processes set in motion at the time of isolation will run their course on most small islands in another few decades. Hyperabundant folivores threaten to reduce species-rich forests to an odd collection of herbivore-resistant plants. Along the way, much plant and animal diversity will be lost. The end-point is likely to be a biologically impoverished system".  Would you say these islands are on this trajectory you described 15 years ago?

    JT: I think it is likely, and I wrote as much in which I showed that the plant community on top of leaf-cutter ant colonies consisted of many plant species that were rare in the flora but apparently resistant to ant foraging.


    HS:  Do you continue to work in these islands? When was the last time you visited them?

    JT: As I said above, in 2003. But by then, the ‘experiment’ had been broken by the drought. I don’t think scientists will be going back to Lago Guri until after the current government has fallen and been replaced with a more outward looking one.


    HS: In the 15 years since this paper was published, have you ever read the paper again? When you read it now, what strikes you the most about it?

    JT: Maybe I read it once. I tend not to dwell on the past.


    HS: This paper has been cited over 1000 times. At the time of its publication did you anticipate that it would have such a big impact? What does it mainly get cited for?

    JT: This is the way the world works. Nothing in that paper is unique to the paper itself. All our results have been published in much greater detail in other publications, of which I now count over 45. Yet, it is the Science article that gets all the citations. My hunch is that a lot of the attention that paper has attracted comes from one word, “meltdown.” Nobody can pass up that word. Had I submitted it with a different, more prosaic title, it might never have been published.


    HS:  Among all the papers you have written, is this one of your favourites? If yes, why?

    JT: I would say, no, because, as I mentioned above, it was merely a summary of a lot of work done by a lot of people. I was only the messenger who wrote it. The paper from Guri that I consider our crowning accomplishment was not published until later: This contained the real meat of the project, the indirect effect of predator loss on the plant community. And the effects were drastic – nearly all plant species in decline under the onslaught of leaf-cutter ants and other generalist herbivores. Yet, we had great difficulty publishing the results. It was rejected by two journals before it was finally accepted. But that was more than 2 years after it had been first submitted.


    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 study published 15 years ago?

    JT: I would tell him/her to read a more recent Science paper I wrote with Jim Estes and others: This is more up-to-date and carries a stronger message about the harm that humans are doing to nature, and the irrevocable changes that humans are causing in ecosystems all over the world





  • Post date: 1 year 7 months ago
    Citation for this post: BibTeX | RIS

    In 1988, , and published in Science developing a model to explain why breeding date in birds, though heritable and under selection, does not evolve. Twenty-eight years after the paper was published, I spoke to Trevor Price about the making of this study, what we have learn since about this topic, and his recent attempts to test this model with breeding bird data from the Himalayas.

     (Interview conducted on 20th July 2016 via Skype)

    Paper citation: Price, T., Kirkpatrick, M. and Arnold, S.J., 1988. Directional selection and the evolution of breeding date in birds. Science, 240(4853), pp.798-799.


    Hari Sridhar: This is the first time you worked on breeding dates in birds. What got you interested in this topic at this point in your career?

    Trevor Price: Being an empiricist beforehand, I wanted to learn theory for my postdoc. When I went to Chicago, Steve Arnold was very interested in sexual selection. This idea about how sexual selection works in monogamous birds was really puzzling a lot of people. , but there was this big question about why, if early breeding females have an advantage, doesn’t breeding keep evolving to an earlier time? Arnold had been puzzling about this and had read in which puzzles about this. Fisher came up with his famous diamond, this explanation for how genetic values can’t be under directional selection even though breeding date can be. Mark Kirkpatrick had just begun this with Steve Arnold, and so I just jumped in really, and puzzled over Fisher’s diamond. We just puzzled over this for about a week, intensively actually, and then Mark said he understood it. That really freaked me out. I spent another day working really hard on this and then I understood it.


    HS: Were you a postdoc. with Stevan Arnold?

    TP: No, I was a postdoc with , the theoretician who put quantitative genetics into evolution. But in classic Lande style, he went off on a sabbatical, for a while, just when I arrived. So I ended up working with Mark Kirkpatrick, who was one of his disciples, and learnt a lot of the theory. Actually, I learnt a lot of the theory from both Russ and Mark. At that stage, Mark had been already collaborating with Steve on how sexual selection in monogamous birds might work. That’s the history of it.


    HS: Were you and Mark Kirkpatrick in different universities at that time?

    TP: Yes, he did his PhD in Seattle, Washington, and then did his postdoc. in Berkeley. He was a at Berkeley but he treated Chicago as his field site. It’s pretty amazing. They kept telling him he couldn’t be away from Berkeley for such extended periods, and he kept pointing out that if you were a field worker you were allowed to go off to Costa Rica, or Panama where was, for six months at a time. So he came up to Chicago for two months at a time, which really was the hot bed of quantitative genetics. We met in Chicago when we were both postdocs.


    HS: But the affiliations on the paper are University of California, San Diego, for you, and University of Texas, Austin, for Mark Kirkpatrick?

    TP: Yeah, that’s right, because we had both finished our postdocs by the time this was published. And we were both just starting our jobs. Obviously, it’s a great thing to do, to have a Science paper in the first year of your job and put your university’s name on it!


    HS: Can you give us a sense of how this collaboration worked? You say the work was done in a week or a couple of weeks…

    TP: No, the work wasn’t done in a week - well, maybe the Science paper was. What was done in a week was very intensive scrutiny of Fisher’s diamond, to try and understand how you can have selection and inheritance but no evolution. Once we figured that out, it was quite straightforward for Mark to write out the model, Steve to come up with the path diagram, which really shows everything, and me to review the empirical literature. But what happened then was we basically put it aside and wrote , which was on sexual selection, and included this little bit as part of it. So we got these two papers on the go, then we submitted the Science paper, and then we went back to the Evolution paper. So we worked on these two papers, while we were postdocs - the big one which had a female preference and the male traits in it, and then this one which was the foundation for that paper. We submitted the Science one first, but while we were still postdocs, Mark started to work on the Evolution one, which uses this and a lot more.


    HS: Did the three of you meet in person to discuss the work that went into this paper?

    TP: Mark and I became pretty good friends, and we discussed it quite a bit. But, in the end, I didn’t really talk much to Steve about it. Steve took a backseat and Mark and I did it. Steve was the motivator for the original idea, Mark and I wrote the manuscript, and then Steve came up with this path diagram – Figure 1. But basically he just let us work on it. The actual manuscripts were written once we had our jobs. I think I basically sat down and wrote a version of this manuscript that Mark then modified and sent back to me. We did it over whatever it was in those days; I guess it was email.  And then we met couple of times and looked over each other’s shoulders when we were doing the writing. This is a pretty simple paper. It is a very simple model in this paper. But we carried on with the same motivation for the big Evolution one. Mark wrote all the equations, all the simulations, that we needed to use for that one. Then I went right through them all and checked them all and then wrote the first version.  I wrote the discussion and the results, then Mark looked at it, and then we got together for the final draft.


    HS: Do you remember how long it took you to write this?

    TP: We put it aside for a while, when I came to work in the field in India. As you know, most papers take a couple of years from beginning to end. My postdoc was 1984-85, and this was three years after that. So, yes, it took 2-3 years to come out. That was partly because I had other things to do, of course. I was finishing up other papers. I don’t know about you, but I find the best way to write a paper is to sit on it for 6 months or so. And with three people, it takes a bit longer as well.


    HS: Where did you do most of the writing?

    TP: I think most of the writing for this particular paper was actually done at Austin. I visited Mark there a couple of times with a draft and we sat down at his computer and wrote it together.


    HS: Do you have a writing routine – a particular time of the day and a place where you like to write?

    TP: Yes, I usually write early in the morning and do my reviews in the afternoon. I can only be reactive by the time it gets to the afternoon.


    HS: You said the motivation for this paper came from Arnold reading Fisher’s work…

    TP: Yes, I don’t know how exactly Arnold came to that, but Arnold was extremely interested in sexual selection and in . You know, the famous runaway sexual selection model of Russ’s? He also, obviously, knew about Darwin’s model, and he must have comes across this diamond in Fisher’s book. Steve wanted Mark to do a model of it, that’s how it came about. But this paper itself has really got nothing to do with sexual selection and the Darwin-Fisher model. In retrospect, I feel it really deserved to be in Science, but most people at the time thought this was a crazy paper to have in Science. It didn’t seem that big. And still many people don’t get how you can have selection and inheritance but no evolution. It’s actually been quoted a lot since, but people still don’t accept that this is one way you can have persistent directional selection on lots of traits. It’s obvious to me. We are all told - presumably you were at one point too - and that’s just not true.


    HS: You say that what you discovered about breeding dates is probably also true of other traits. Subsequent to this paper, have other traits been discovered?

    TP: Yes, I think so. Of course, . Body size is another classic trait actually, which seems to be under persistent directional selection. You know if you look at a lot of of selection you find a lot of traits are under strong directional selection over their whole life history. And yet people still puzzle over that, they still say: ‘Well, they have got some unmeasured trade-off somewhere else in their life history’. But I’m pretty certain they haven’t. I’m pretty certain that it’s this phenomenon. So nearly all sexually selected traits, for example, we predict to be condition dependent. They should evolve to be condition dependent and as soon as they evolve to be condition dependent you get this phenomenon. Now what that does is it creates directional selection on the trait. But there’s a balance you see:  you’ve got stabilising selection on the genetic component, directional selection on the non-heritable component, which sometimes can lead to stabilising selection when measured over the whole life history, but often it will lead to directional selection over the whole life history. So nearly all sexually selected traits are probably subjected to this kind of thing. In fact, most traits you can think about have got some kind of condition dependence in them.


    HS: Was this the first piece of theoretical work you did?

    TP: Yes, absolutely. This is how I learnt quantitative genetics theory. I started off working with Russ trying to do a theoretical model of reinforcement, but that had hybridisation in it, which rapidly creates non-normality. Non-normality is Russ’s biggest nightmare. In the end . So this was the first piece of theoretical work I did.


    HS: Since then you have done a lot of theoretical work. Do you enjoy that as much as doing empirical work in the field?

    TP: I think what I like about theoretical work is I do it very rarely. I mean I do theory, but the number of papers I have written on my own is tiny. I really enjoy working with very smart theoreticians and solving problems that have been an outstanding mystery to me. I do really enjoy the light forming in front of my eyes when something like this is solved. I mean, it was a puzzle for a long time and now we understand it. So I’m carrying on in that way even today, working with theoreticians on issues I can’t understand, which become clearer when they model them. So that I enjoy. But I wouldn’t say I enjoy it as much as fieldwork, because that I do on my own.


    HS: Did this paper have a relatively smooth ride through peer-review? Was Science the first place you submitted it?

    TP: No, we submitted it to Nature first. We got rejected, we appealed, and the appeal was accepted. But then it got rejected again. Then it also got rejected at Science, the first time. But Mark already had a name for himself, and so the editor at Science actually called him up and said: ‘Why should we publish this?’ I think Mark did a very good PR job on it. Despite all this, I think this paper probably had a smoother ride than many of my other papers.


    Hs: Was the final published version very different from the first submitted draft?

    TP: No, it didn’t change much. I mean, with three people working on it you know, it was pretty good.


    HS: Did this paper attract a lot of attention when it was published?

    TP: You know those were different days. A paper in Science tended to attract attention. There weren’t 10 other journals and only about 10% of the science being done now. So it attracted a fair bit of attention, but many people just couldn’t understand why this was in Science. I think people do now.

    I should also say, one of the reasons I’m resurrecting the work at the moment is we have got a lot of interesting data on breeding dates of birds in Himalayas. Figure 2 in this paper shows that there should be a mismatch between breeding data and optimal time to breed. I am sure you are aware of this: people will talk about how a mismatch induced by climate change is causing bird reproductive stuff to go down. But it is not quite as simple as that because it turns out the optimal timing can be a mismatch. And this second part of the paper basically has not been played up at all. Figure 2, which shows this mismatch, has not been discussed in the literature very much. So I’m now trying to do models and use empirical data from the Himalayas to show mismatches are often optimal. You can’t actually interpret a mismatch as bad. What people do is they measure the average breeding date of the bird, but what natural selection is doing is working on the average breeding date of all the offspring that are produced. And birds that breed earlier in the season produce more offspring because they are in higher condition. So there’s stronger selection on those birds. Therefore, if you actually were to reformulate it as the distribution of surviving offspring they would lie right under the optimum. In this paper, we didn’t discuss why it should be that birds that breed earlier should be in higher condition. We just said we are leaving that bit aside. Now, I’ve worked out the full model which shows that birds in higher condition should breed earlier, but also calculates what the mismatch should be, under different selective conditions. That’s what we are working on right now. We have got 25 years of data from the Himalayas about how breeding date is moving forwards. There are a lot of ramifications of this whole thing. One of the things we don’t talk about is why high condition birds breed early, and we now know why that is. Another important point is that high condition birds should impart that condition to their offspring, so you expect maternal effects. Maternal effects are not in this paper either. Now, we have built the complete model where birds in different condition produce different numbers of offspring. And we have shown where the breeding date should evolve to and how much of mismatch that should produce. And the empirical data from the Himalayas is really showing that this condition effect is very important. But it’s still a long way from being published.


    HS: What kind of impact did this paper have on your career? How did it influence the future course of your research?

    TP: On my career it didn’t have any impact, in terms of things like tenure. People just said: “Oh, that was before you got here” and stuff. But in terms of my research it had a strong impact. I wrote and how you could get an optimal clutch size in a similar way. Everyone was talking about optimal clutch size at that time. A lot of the theory I have done since was coming out of extending this model and building on it. I had one very influential paper with where we put condition effects into sexually-selected traits. and has been widely quoted. So, basically, this was foundational for my understanding of quantitative genetics, and subsequent theory I did, and which I have been doing ever since.


    HS: In general, would you say that what you propose in this model holds true even today? If you were to rewrite this paper today would you change anything?

    TP: That’s a very difficult question. At that time we just said we do not discuss why birds in high condition should breed early. I think if we write the paper today, people will say you have got to discuss that. But we just didn’t know why then. Now we do. So it will be a longer, more complicated paper. That’s the trouble. But there’s nothing in the paper that’s wrong.


    HS: You say “It is not known whether the average breeding date actually is later than the ecologically optimal time for raising young in natural populations”. I’m guessing you have a better idea about this now, at least from the Himalayas?

    TP: It’s always advantageous to an adult’s survival to breed as early as possible because you can go through your moult and come back. So that may push breeding date before the optimal time for raising young. Birds that breed very early are going to have higher survival because they can just simply get through the season quicker and get ready for the winter. So we’ve got two forces acting here: the condition effect which pushes breeding date later, and a trade-off, a genuine trade-off between high fecundity and high survival. What we haven’t worked out in the model yet is how these two conflicting things, this condition effect and the breeding date effect, resolve themselves. So putting everything together you get these two effects, one is pushing you before the optimal and one is pushing you after. But in the Himalayas, it looks like it’s resolved to be before the optimal. For example, the , which is a bird we study, breeds early. In contrast, the comes back later, is in the same habitat, but breeds 2-3 weeks later. It seems to us that the greenish warbler is breeding when food is optimal. So I don’t know if its competition or if it’s just simply that yellow-browed leaf warblers are smaller, so it can do with smaller food items and less food. But it breeds before the greenish warbler and the food abundance still seems to be increasing when the greenish warbler breeds.

    I don’t really understand the European tit studies, in the light of what goes on in the Himalayas. European studies have measured caterpillar frass and shown a mismatch. But tits breed even earlier in the Himalayas than warblers do. There’s relatively a small amount of food out by the time they are raising their young. So I don’t really understand the European studies that talk about mismatches.


    HS: Apart from the Himalayas, is there data on this from other parts of the world?

    TP: There’s lots of data but it is nearly all based on nest box studies. Nest box studies have a number of issues, but it’s hard to criticize them because the people who do them review your papers. But there are two big issues. One is that they are relatively predation free. The other, probably the more important one, is that the densities are artificially increased. So you’ve actually got all sorts of weird things going on. There are studies in tits all over Europe, studies on parrots in South America and studies on swallows in North America. They have all used nest boxes, changing the densities of the bird populations they are working on and cutting out predation. So I just don’t know how relevant they are.


    HS: You say that earlier studies “confound the effects of the environment [] and the effects of nutrition [] on female fecundity” and “It will be critical to distinguish these two effects” when investigating selection on breeding date. Has this happened?

    TP: Yes, people have tried. There was, actually, stimulated by our paper, for about 10 years, massive attempts to do that. So there was really an attempt to test the model, . And the idea was that you would not be changing condition but you would be changing breeding date. Other cases where they tried to change condition by plucking feathers from adults. So there was a lot of work on that, but I think it’s all been very inconclusive. It’s been very hard to do, especially when you didn’t have the full model. We didn’t have the model to explain why high condition birds should breed early. So I think now, with the full model, that could be revisited. It’s also been very difficult to separate the two effects. It might be now, now that we have got the full model, but I think it still probably would be very hard to do. The full model has this trade-off, where if you breed early you get an advantage, and I don’t think that trade-off was in the thinking of these early papers. But there were a flurry of empirical tests that, you know, were quite ingenious, but they have either been equivocal or they have done what you might predict, which is show that both condition and direct effects of breeding date are important.


    HS: Could you tell us a little more about the people you acknowledge – how you knew them and how they helped?

    TP: They all read and commented on a draft of the paper. and were both postdocs in Chicago and good buddies of mine. was my PhD supervisor, was a colleague in San Diego, and and I were graduate students together. In fact, at that time, Dolph and I were sharing every paper we wrote.


    HS: Do you remember if the grants you mention were specifically for this paper?

    TP: Let me look. Ah, they weren’t grants to me. That’s a familiar story! Two grants to Steve and they were not for this work at all; they were for salamander work. And Mark’s grant was to do quantitative genetics in sexual selection, which is what he ended up doing. He had a whole bunch of papers on handicap and things like that, at that time.


    HS: Is this analysis with the Himalayan data the first time you are testing this model?

    TP: Yeah, that’s right. After this paper, I basically went off and did stuff for the . We were trying to do quantitative genetics but it was really hard. But we did have . It was looking at the wing bar. So, no, we didn’t ever try and test it earlier, although it could have been a focus of my work. I was just caught up in the phylogeny stuff.


    HS: Have you ever read this paper after it was published?

    TP: I think I probably have, for one reason or the other. When I have been teaching classes and so on. You know, I like this paper. It’s very short of course, extremely short. Some of my papers I read and think they are horrible, but some papers you read and think: “God, I was really thinking very deeply about that. About issues I have completely forgotten about.” This one’s like that. It’s got stuff in it that I have completely forgotten. And I think it was a pretty good paper at the time. But that’s going to happen when you work with two really smart people.


    HS: Do you think your writing has changed since the time of this paper?

    TP: I have no idea. I mean we would all like to think we are getting better at these things. I probably think my creativity has gone down. That paper was much more creative than the ones I’m doing now. But that’s why I work with students. They are the creative side, and I try and write the paper so it’s accessible to people. My writing has probably gotten better, but not much. It’s always hard, man. Writing papers is hard. But one thing that does happen is that there’s not the same pressure to work fast. It’s getting a bit ridiculous, but the two papers I’m working on with theoreticians at the moment, we started over 5 years ago. Today, I am able to put it aside, do other things, come back to it and make it better. . By the time you get to the last chapter, its two years since you wrote the first chapter, so you’ve had that time to revise and get things right.


    HS: What does this paper mostly get cited for?

    TP: I know what happened. It sort of didn’t get cited for a while, and then " target="_blank">the Oxford group that studies tits, and the , got very interested in this question about lack of evolution of breeding dates. So I would say it’s mostly cited for what it says. But people still don’t believe it. You will often see a list of six reasons why heritable traits won’t evolve and ours will be number six, and they are still trying to sort out which one it is. I would say it’s cited mainly because the Oxford and Finnish groups got interested in it. Also now, there is interest in it in the context of breeding date and climate change.  



    HS: What would you say to a student who is about to read this paper today? What should he or she take away from it?

    TP: It’s still really relevant today. But of course, there is this big big chunk missing, which is: why birds in high conditions should breed earlier or be bigger or have longer tails. A lot of unfinished work. So if you are reading this paper today, make sure you understand why heritable traits don’t evolve, and then go back to the literature of the last 30 years to understand why condition correlates with these traits.  


    HS: Among all the papers you have written, is this one of your favourites?

    TP: No, not really. My favourite papers are probably the empirical ones like . And usually, the one I have just written! I started out doing correlative field work and then I had theoretician envy, but now I appreciate that its experimental work, really, where the skill lies. I still haven’t written a paper that’s got an experiment in it, so I would like to do that. But I think my favourite papers are basically the ones where it involved some field work and I learnt something directly about nature.


  • Post date: 1 year 7 months ago
    Citation for this post: BibTeX | RIS

    In 1992, and Harold Welch published in Marine Ecology Progress Series in which they use isotopic analysis to show that the food web in the Barrow Strait–Lancaster Sound area in the Arctic consists of five trophic levels. This was one of the early studies that used isotopes to determine trophic levels. Twenty-four years after the paper was published, I asked Keith Hobson (with inputs from Harold Welch) about the making of this paper and what we have learnt since about the food web in this area.

    Hari Sridhar: Correct me if I'm wrong, but this seems to be only your second paper on food webs. What got you interested in food webs at this stage in your career? What was the motivation to do this study?

    Keith Hobson: Our motivation originally was to study ecological segregation among seabirds in the high Arctic. We realized that stable isotopes could be used for this purpose, but that an understanding of the stable isotope values in many of the food web components would be needed to decipher the seabird isotope data. So, the isotope technique forced me to take a full food web approach from primary production to seabirds. Of course, while involved in this aspect, adding marine mammals was an obvious opportunity and so we ended up studying phytoplankton to polar bears.

    HS:  In the paper you say "this area has received considerable attention from marine ecologists owing to its projected use as a transportation corridor and the potential development of the region's hydrocarbon and mineral reserves". Was this also part of your motivation for this study? Has the region been put to use for transportation and resource extraction, as was expected then?

    KH: I have always been driven by a strong conservation ethic and remain deeply concerned about the future of nature on our planet. The Lancaster Sound region of the Canadian high Arctic has always been a focus of potential resource extraction and, now that climate change is happening rapidly, the between the Atlantic and Pacific will become a reality with all of its attendant exploration and resource development. So, while major development has not occurred, likely due to low oil prices etc., the eventual development in the region is more likely now than ever.

    HS: This paper is "Contribution No 17 from the Resolute Marine Laboratory". Does this laboratory still exist?

    KH: Unfortunately not. It was closed not long after my own work there. Harold Welch was the Director of that facility and he might be able to tell you how many publications came out from this lab. [Harold Welch adds: I have no idea how many papers came out of the Resolute lab but around 25 would be my guess.]

    HS: How did the collaboration between you and Professor Harold Welch come about? What were your respective roles in this project? Did you continue to work with Professor Welch after this paper?

    KH: Dr. Welch ran the laboratory for the and I was allowed to use the facility as a logistical base for my PhD thesis with the University of Saskatchewan. Dr. Welch was also an expert in marine food webs in the High Arctic. I have continued to work with Dr. Welch over the years through his retirement about 12 years ago. We are good friends and colleagues.

    HS:  Can you give us a sense of the fieldwork - what was a typical day in field like, where did you stay, how many people were involved in sample collection, did you set up a lab in field etc.?

    KH: The laboratory also provided accommodation and was located in the small hamlet of Resolute Bay. From that logistical base, our food web sampling was done from small powerboats locally and a larger research vessel the “Ogak” which is Inuit for “Arctic Cod”. Those sampling trips could be days to weeks. The seabird work was conducted primarily from remote field camps, from tents, and could last for weeks to months. Transport to those camps was by helicopter or Twin Otter. So, much of the work was logistically very challenging and involved lots of concerns about weather and polar bears!

    [Harold Welch adds: The Arctic can be an unforgiving place. Keith's supervisor, , died tragically in a helicopter crash, along with another close friend and colleague.  Subsequently, , who learned his stuff as my graduate student, died in another plane crash in Resolute, after becoming head of the (PCSP) that supports Arctic research.

    Once, Keith, I and two others were returning in a seven meter boat, from Devon Island about sixty miles away, when the fog rolled in.  We navigated through the ice as best we could and finally, just about out of gas, we drove up onto the sea ice to spend the night, without a clue as to where we were.  But the fog lifted several meters and I recognized an island where I'd built an iglu, and we made it home on fumes that evening.  It was routine, but it made a big impression on Keith.]

    HS: If you did this study again today would do it differently, given the development in technology and analytical techniques?

    KH: I do not think we could improve much on the field sampling, but of course more money and resources could always lead to more samples. However, the type of analyses conducted at the isotope lab would likely change, and now include also compound specific isotope analyses of amino acids and fatty acids in addition to the bulk tissues (muscle, feathers etc.) we looked at.

    HS: How long did the writing of this paper take? Who did most of the writing? During the writing phase, did you and Professor Welch meet often or were discussions mostly over the phone?

    KH: I did most of the writing because this work formed a substantial part of my PhD thesis. That likely took about two months, once all the isotope data was secured. However, Dr. Welch provided valuable expert advice and we discussed the various drafts of the paper primarily in person. After my PhD, I spent 6 months with Dr. Welch at the , as a postdoc.

    HS:  Where did you do the writing - in your field station/ in your office/ in the university/ at home etc.? Do you have a writing routine?

    KH: At that time, most of the writing was done at my office in the University of Saskatchewan. I will write anywhere that is quiet and away from distractions.

    HS: How were the figures for this paper drawn? Who drew them?

    KH: In those days, I did not have access of the wonderful graphics programs available today. So, the graphics are crude by today’s standards. However, I prepared all figures with assistance from a Departmental graphics person (those positions likely do not exist anymore or are rare). 

    HS:  Some questions about the Acknowledgements: what was the Polar Continental Shelf Project? Who was M.A. Ramsay, who obtained a grant for this project? Can you tell us how you knew each of the people who helped you in field, with identification and with illustrations (N. Grant)?

    KH: The Polar Continental Shelf Project is a Canadian government funded institute to facilitate research work in the Canadian Arctic.  Ramsay was a polar bear biologist who was also my PhD supervisor at the University of Saskatchewan. He has since died in a helicopter accident while working on polar bears. Amamalik and Amarualik were Inuit assistants who lived in Resolute Bay. Bergmann and worked for Harold Welch as research assistants. Graham was director of the Vancouver Aquarium at the time and helped with field collections. Hop was a fellow PhD student working on Arctic Cod. Martin was the captain of the research vessel Ogak. Curtis and Frank were museum experts who helped identify specimens. Grant was a graphics person who worked in the Biology Department, University of Saskatchewan.

    HS: Did this paper have a smooth ride through peer review? Was Marine Ecology Progress Series the first place you submitted this to?

    KH: The paper was only submitted to this journal and I recall it was well received and required only one revision before being accepted.

    HS: In your paper you use a value of +3.8% for the Delta15N enrichment factor between trophic levels. Has there been improvement in our ability to estimate this value? What is this value now, for this system?  Also, is the method used to calculate trophic level
    still the same?

    KH: Rather remarkably, this value has held up well. Meta-analyses of many food webs now places the value closer to 3.4 per mil, but I still find the best evidence supports our earlier estimate. Then again, this value was generalized for the whole food web and we really did not expect that it would apply precisely to every trophic step. We used this value to model the food web off west Greenland just recently and it continues to make sense. However, the trend today is to use stable nitrogen isotope analyses of individual amino acids to model trophic positions. That work is much more involved, analytically, and, of course, is much more expensive, but will likely provide the most accurate data in the long term.

    HS:  You say "to expect a consistent isotopic enrichment factor between all trophic levels is inappropriate" Do we have a better understanding, today, of specific isotopic fractionation factors between trophic levels? You also highlight the need for "Controlled laboratory determine isotopic fractionation values between primary producers and herbivores in this system" - has this happened?

    KH: As stated above, it remains unrealistic to suppose there is a universal enrichment factor that could be applied equally to all consumers and we, in fact, know this is not the case. Controlled laboratory studies have continued to some degree but I would like to see more. We now know that these factors can be influenced by the nutritional quality of diets and so researchers must be careful to take this into account when dealing with captive animals raised on homogenous diets. Specifically, I would say that our knowledge of the specific factors influencing isotopic discrimination between primary productivity and herbivores remains poorly known.

    HS:  Is the model of this food web the same today or has it changed -  Is the number of levels different? Is the ordering of species different? Have more species been added with more research? Have species been removed because of local extinctions?

    KH: In general terms, the food web remains unchanged with about a five trophic level system separating polar bears from primary productivity. I am unsure if species composition has changed, and I would guess that there have been no follow-up studies conducted in the region since our original work. So, little information would be available to detect any extinctions per se. The key players are the copepods, amphipods, arctic cod, seabirds and marine mammals. With climate change, the food web is poised to change.

    HS: In your paper you say "We predict that seals taken later in the autumn, after the major onshore movement of Arctic cod, will show tissue isotope values more enriched in Delta15N". Has support for this been found in later work?

    KH: To my knowledge, this has not been investigated. With the closure of the DFO research station, I am afraid there seems to have been little incentive for any follow up work.

    HS:  Towards the end of your paper, you emphasize the need for isotope work that is across seasons and year-round, that targets various age classes of animals, and that uses several tissue types. Has this happened?

    KH: This has happened in other parts of the Arctic. The . That study used multiple tissues and sampled from a Canadian Coast Guard vessel intensively from early summer to late summer. I suspect, but do not know for sure, the Norwegians have pursued this question more off Svalbard, using identical procedures but with more year-round sampling. Logistically, it is still extremely difficult to sample food webs in winter beneath the sea ice.

    HS:  Are Arctic cod and lower trophic-level invertebrates still critical in this food web?

    KH: Most definitely yes, as they are the link between amphipods and copepods and piscivorous marine mammals and seabirds. Having said that, I was very impressed by the direct use of zooplankton by many of these “upper trophic level” groups.

    HS:  In your study, and other studies around that time, there was a lack of strong enrichment of DeltaC13 beyond the first trophic shift. Do we now have a better understanding of why that is so?

    KH: There continues to be much evidence for small trophic enrichment effects for carbon vs nitrogen stable isotopes. This is linked to the kinetics of fractionation and the number and magnitude of the steps involved in the construction of animal tissues from diet. Amination and deamination of proteins and the subsequent voiding of nitrogenous waste strongly fractionates biochemically for nitrogen isotopes. The opportunities for fractionation are simply less and of lower magnitude for carbon isotopes in these reactions. So, it is not so much why the carbon isotope discrimination is low trophically but why the nitrogen isotope discriminations are so high.

    HS:  Did the paper attract a lot of attention when it was published?

    KH: Eventually, but I would say that it really took a few years to be recognized appropriately, as the first isotopic delineation of a full length food web of this magnitude.

    HS: At the time this was published, did you anticipate that it would be cited so much? Do you know what this paper has been mostly cited for?

    No, I did not anticipate it would stand the test of time so well. I think it is primarily cited as a classic example of how powerful the stable isotope approach can be in modeling food webs. To some degree, it also is cited to illustrate the importance of lower trophic level zooplankton in arctic marine food webs.

    HS:  What impact has this paper had on your research and your career? Did it open up new lines of investigation?

    KH: This paper led to continued links with high latitude marine food web research. I have continued such work in the Gulf of Alaska, the northeast and northwest of Greenland. In more recent years, my food web research has focused more on freshwater systems and the use of new isotopes such as those of hydrogen. The general notoriety of the work certainly helped me to develop my career using stable isotope methods. That work now has moved on more to tracing migration.

    HS: What would you say to a student about to read this paper today? What should he or she takeaway from it? Would you add any caveats?

    KH: I think students today must see the paper in context. This was the very first attempt to see if stable isotopes could be used to model whole complex food webs. Before this paper, there really was no straightforward modeling of food webs using stable isotopes. All new and original and aimed at the “big picture” or overview. As I indicate below, technology at the time was also not what it is today and so sample sizes were often limited. Students have a much more convenient means of using stable isotopes in their research today. I would also say that the approach was not without its risks of failure and so it can pay to take chances in planning research questions.

    HS:  Have you ever read the paper after it was published? When you read it now, what strikes you the most about it?

    Of course, I am flooded by good memories of the Arctic, the field sites, the animals and the people I worked with. I think scientifically it is still very sound and impressive. The big difference might be that, today, one would expect larger sample sizes, because the technology used to analyse samples isotopically has changed so much. Samples had to be prepared and run individually (by me) in the early days. Today, the systems are automated and students would simply submit their samples to a lab and sample throughput would be comparatively fast and less expensive.

    HS: Is this your favourite paper among all the papers you have published? If yes, why? If no, and if you do have another favourite, which is it and why?

    KH: Yes, it is definitely one of my favorites. The other competitor would be the early papers (, ) we published on tracking the migration of monarch butterflies using stable hydrogen isotopes. Both research projects were just so different from anything that preceded them!

    HS: Do you still work in this field site? How has it changed since the last time you worked there?

    KH: No, since the laboratory in Resolute Bay was closed, no further work has been possible. I am sure I would notice a big difference if I returned, as many have commented on the way in which the climate has changed.


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